Accepted Manuscript

Bisphenols: Application, Occurrence, Safety, and Biodegradation Mediated by

Bacterial Communities in Wastewater Treatment Plants and Rivers

Magdalena Noszczyńska, Zofia Piotrowska-Seget

PII: S0045-6535(18)30397-7

DOI: 10.1016/j.chemosphere.2018.02.179

Reference: CHEM 20937

To appear in: Chemosphere

Received Date: 02 November 2017

Revised Date: 06 February 2018

Accepted Date: 28 February 2018

Please cite this article as: Magdalena Noszczyńska, Zofia Piotrowska-Seget, Bisphenols:
Application, Occurrence, Safety, and Biodegradation Mediated by Bacterial Communities in
Wastewater Treatment Plants and Rivers, Chemosphere (2018), doi: 10.1016/j.chemosphere.
2018.02.179

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 ACCEPTED MANUSCRIPT

1 BISPHENOLS: APPLICATION, OCCURRENCE, SAFETY, AND

2 BIODEGRADATION MEDIATED BY BACTERIAL COMMUNITIES IN
3 WASTEWATER TREATMENT PLANTS AND RIVERS

4 Magdalena Noszczyńskaa*, Zofia Piotrowska-Segeta

5
6 aDepartment of Microbiology, University of Silesia, Jagiellońska 28, 40-032 Katowice,
7 Poland
8 *Corresponding author: magdalena.noszczynska@us.edu.pl; 0048 502 301 521
9
10 The e-mail address of second author:
11 zofia.piotrowska-seget@us.edu.pl

12 Keywords: bisphenols, biodegradation, bacteria, wastewater treatment plant, river

13
14 Abstract

15 Numerous data indicate that most of bisphenols (BPs) are endocrine disrupters and

16 exhibit cytotoxicity, neurotoxicity, genotoxicity and reproductive toxicity against

17 vertebrates. Nevertheless, they are widely applied in material production what result in

18 their ubiquitous occurrence in ecosystems. While BPA is the most frequently detected in

19 environment, BPAF, BPF and BPS are also often found. Ecosystem particularly exposed

20 to BPs pollution is industrial and municipal wastewater being a common source of BPA

21 in river waters. Different techniques to remove BPs from these ecosystems have been

22 applied, among which biodegradation seems to be the most effective. In this review the

23 current state of knowledge in the field of BPs application, distribution in the environment,

24 effects on animal and human health, and biodegradation mediated by bacterial

25 populations in wastewater treatment plants and rivers is presented.

26

27 1. Introduction

28 In the last two decades there has been a growing awareness of the possible unfavorable

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29 effects on humans and animals health resulting from exposure to endocrine disrupting

30 chemicals (EDCs). Among EDSc, bisphenol A (BPA) is the most important synthetic

31 chemical. BPA has received enhanced attention in the last few decades because of its

32 widespread application in many industries (Ye et al., 2009). Other bisphenols (BPs)

33 called BPA-related compounds or bisphenol analogues also have a wide range of

34 applications in material production. Some of them are considered to be able to partially

35 replace BPA in the industrial applications. Nevertheless, numerous studies revealed their

36 endocrine disrupting effects, genotoxicity, neurotoxicity, and cytotoxicity in laboratory

37 studies (Chen et al., 2016).

38 The widespread application of BPs results in their still growing discharge into the

39 various environment compartments including indoor dust, surface water, sediments and

40 wastewater (Liao et al., 2012a, 2012b; Liu et al., 2017). The latter is one of the main

41 source of BPA causing its widespread and variable occurrence particularly in urbanized

42 area (Michałowicz, 2014). BPA was detected both in influent and effluent of wastewater

43 treatment plant (WWTP) in concentration from 60.5 to 1960 ng L-1 and from 5.2 to 138

44 ng L-1, respectively (Zhou et al., 2010; Sun et al., 2017). Moreover, the effluent is a

45 major source for BPA entering rivers (Zhao et al., 2008). Other bisphenols such as BPS

46 and BPF are also frequently found in WWTP.

47 Presently, several methods have been developed for the removal of BPA from aqueous

48 solution included biochemical oxidation, absorption, electrochemical oxidation,

49 ozonation, Au-Fenton catalysts and biodegradation (Kang et al., 2006; Yang et al.,

50 2013). Among these techniques, biodegradation has been demonstrated to be an effective

51 method to remove BPA from water (Zhang et al., 2013). Biodegradation has been also

52 considered as promising method to remove other BPs and reduce their toxicological risk

53 (Danzl et al., 2009; Sakai et al., 2007). In addition, several bacteria distributed in WWTP

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54 as well as in river water are capable of readily degradation of BPA. Studies concerning

55 BPs have mainly focused on the isolation and characterization of single bacterial strains,

56 while in the natural environments, contamination removal is conducted by a whole

57 microbial community, instead of a single isolated degrader (Xiong et al., 2017b).

58 The aim of this review is to compile the current state of knowledge on the application,

59 occurrence in environment, endocrine, and toxicological effects of BPs, and to collect

60 findings in the field of bacterial groups involved in degradation of bisphenol analogues,

61 particularly BPA in wastewater treatment plants and rivers.

62 2. Bisphenols

63 2.1. Application and occurrence in environment

64 Among bisphenols, most commonly used in industry is BPA. It is made up of two

65 methyl functional groups connected by a bridge with two unsaturated phenolic rings

66 (Staples et al., 1998). Commonly use of BPA resulted in its annual production estimated

67 a 8 million metric tons in 2016 and projected to reach 10.6 million metric tons by 2022

68 (Bisphenol A, A Global Market Overview, 2016). It is applied in the production of

69 durable and heat resistant food containers, water pipes, sport safety equipment,

70 protective and corrective eyewear, eyeglass lenses, medical equipment and tubing,

71 thermal papers and many plastic consumer products including toys as well as compact

72 discs and DVDs (Bisphenol-a.org, 2016; Björnsdotter et al., 2017). Polymers made from

73 BPA can be hydrolyzed under high temperature and in acidic and alkaline pH conditions,

74 causing BPA leaching into water, food containers and also baby feeding bottles

75 (Chouhan et al., 2014). The BPA exposure estimate to be from 0.48 to 1.6 μg kg−1 body

76 mass per day, for adults and children, respectively (Flint et al., 2012). Due to increased

77 concerns over the safety of BPA, in many countries BPA regulation has been tightened.

78 For example, in United States (U.S.) and European Union, the use of BPA-based

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79 Polycarbonate (PC) resins in baby bottles and spill-proof cups was prohibited. In

80 Belgium and Denmark, BPA was banned in food contact materials and articles for

81 children under 3 years (Modern Testing Services -Global, 2013). In France from 2015,

82 the use of BPA in all packaging, containers and utensils intended to come into direct

83 contact with food was prohibited with the exception of food containers destined for the

84 export market (Bisphenol A, Euroactiv, 2015). Beyond BPA, another bisphenol

85 analogues have been documented for industrial applications. Bisphenol AF [BPAF; 4,4'-

86 (hexafluoroisopropylidene)diphenol] is used as a crosslinking agent for certain

87 fluoroelastomers, as a monomer for polyimides, polyamides, polyesters, polycarbonate

88 copolymers and food-contact polymers (Feng et al., 2012). Bisphenol AP [BPAP; 4,4´-

89 (1-phenylethylidene)bisphenol] is used as the start material of polyester, polyether, and

90 polycarbonate (Wang et al., 2011). Bisphenol B [BPB; 2,2-bis(4-hydroxyphenyl)butane]

91 is applied in the manufacture of phenolic and polycarbonate resins (Yoshihara et al.,

92 2004). Bisphenol F [BPF; 4,4'-dihydroxydiphenyl-methane] is used to make epoxy resins

93 and coatings for various applications, such as lacquers, varnishes, liners, adhesives,

94 plastics, water pipes, dental sealants, and food packaging (Bisphenol F, Toxicology Data

95 Network, 2013). Bisphenol S [BPS; 4,4 ́-dihydroxydiphenylsulphone] is increasingly

96 used as replacements for BPA in the production of polymers (e.g. baby bottles,

97 microwave dishes, dialyzers, coatings, etc.) as well as a raw material in the preparation

98 of a number of products (e.g., fire retardants, developers for heat sensitive paper,

99 intermediates for colorants, pesticides) (Bisphenol S, National Toxicology Program,

100 2014). No usage data are available for other BP analogues, however some studies

101 suggested that they production and application are on the rise globally (Chen et al.,

102 2016).

103 So far BPA, BPAF, BPAP, BPB, BPF, Bisphenol P [BPP; 2,2-bis(4-hydroxy-3-

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104 methyl)phenylpropane], Bisphenol Z [BPZ; 4,4′-cyclohexylidenebisphenol] and BPS

105 have been detected in the various environments. These BPs were identified in indoor

106 dust samples collected from the U.S., China, Japan, and Korea. The total concentrations

107 of bisphenols (∑ BPs; sum of eight BPs) in dust were in the range of 0.026 - 111μg g-1.

108 Among individual bisphenols, BPA and BPAF were the predominant compounds (Liao

109 et al., 2012a). Another studies have reported that the median concentration of ∑ BPs in

110 selected country was the lowest in Pakistan 0.15 μg g-1 and the highest in Greece 4.48 μg

111 g-1 (Wang et al., 2015). In surface sediment collected from industrialized areas in the

112 U.S., Japan, and Korea, the highest ∑ BPs concentration ranged from below the limit of

113 quantitation to 25 300 ng g-1 dry weight (dw). The highest concentrations of both

114 individual and total BPs were in sediment samples from Lake Shihwa in Korea. The

115 most commonly detected was BPA followed by BPF (Liao et al., 2012b). In sediment

116 samples from Taihu Lake in China, the ∑ BPs in 2013 ranged from 0.37 ng g-1 dw to 8.3

117 ng g-1 dw (Jin and Zhu, 2016). Compared to the data of BPs concentrations in the

118 sediment collected in 2016, the concentrations of each BPs increased. The ∑ BPs were in

119 the range of 23 - 4.3 × 102 ng g-1 dw. In waters samples from Taihu Lake, except BPA,

120 BPF and BPS were two other major BPs (Liu et al., 2017). BPs were also reported in

121 WWTP (Table 1). In China, BPA, BPAF, BPE, BPF, and BPS were widely detected in

122 influent and effluent with the average concentrations:1960; 0.901; 4.51; 35.8 and 55.7 ng

123 L-1 in the influent, 231; 1.16; 4.07; 1.67 and 0.596 ng L-1 in the effluent, respectively

124 (Sun et al., 2017). The BPs levels in the sludge were within the similar ranges as these in

125 Korea and USA (Lee et al., 2015; Yu et al., 2015a). In Korea, the presence of BPs in

126 sludge obtained from both industrial- and domestic-WWTPs were demonstrated.

127 Interestingly, while BPA dominated in the sludge from industrial WWTPs, sludge from

128 domestic WWTPs was contained elevated proportions of BPF. This indicated the

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129 existence of a specific source of BPF in domestic sources like water pipelines (Lee et al.,

130 2015). Moreover, BPF was the most abundant bisphenol analogue in surface water from

131 some sites in China, Korea, and Japan, suggesting that BPF was the major BPA

132 replacement in southeastern Asian regions (Yamazaki et al., 2015).

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133 Table 1
134 Comparison of BPs in wastewater from WWTP [ng L-1], river water [ng L-1] and sludges [ng g-1 d.w.] from selected countries

135
Source Country BPA BPAF BPAP BPB BPF BPP BPS BPZ References
136
Wastewater - influent China 1960 0.901 NA <LOQ 35.8 NA 55.7 NA (Sun et al., 2017)
Wastewater - efluent China 231 1.16 NA NA 1.67 NA 3.02 NA (Sun et al., 2017)
137
Wastewater - influent India 60.5 1.1 0.3 2.5 10.4 7.8 14.7 0.6 (Karthikraj and Kannan, 2017)
138 Wastewater - efluent India 5.2 ND ND 0.6 0.6 0.8 2.4 ND (Karthikraj and Kannan, 2017)
Sewage sludges China 477 7.45 NA NA 70.09 NA 2.25 NA (Sun et al., 2017)
139 Sewage sludges India 5.6 ND ND ND 8.2 ND 185.7 ND (Karthikraj and Kannan, 2017)
Sewage sludges China 4.69 0.85 NA NA 3.84 NA 3.02 NA (Song et al., 2014)
140 Sewage sludges Korea 1050 0.70 ND ND 699 2.53 63.4 ND (Lee et al., 2015)
Sewage sludges US 459 6.01 <LOQ 0.97 17.2 1.06 34.5 1.81 (Yu et al., 2015b)
141 Liaohe river China 47 1.9 0.0035 ND ND NA 14 0.054 (Jin and Zhu, 2016)
Hunhe river China 40 2.4 ND ND ND ND 11 ND (Jin and Zhu, 2016)
142 Han river Korea 141 NA NA NA 633 NA 41 NA (Yamazaki et al., 2015)
Korttalaiyar river India 33 NA NA NA ND NA 8.7 NA (Yamazaki et al., 2015)
143 Edogawa river Japan 14 NA NA NA 340 NA 3.4 NA (Yamazaki et al., 2015)
Liaohe river China 0.14 0.0016 0.022 ND 0.034 NA 0.092 0.050 (Jin and Zhu, 2016)
144
Hunhe river China 1 0.0017 0.026 ND 0.92 ND 0.0073 0.060 (Jin and Zhu, 2016)
145 NA – not analyzed, ND – not detected, LOQ – below the limit of quantification
146
147

148

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149 Interestingly, the presence of BPA, BPF and BPAF in soil samples collected from

150 agricultural fields and industrial soils in Spain was detected, however, only the levels of

151 BPF and BPA could be quantified. The presence of bisphenol analogues in the soil was

152 linked with the use of reclaimed waters for irrigation of agricultural fields (Pérez et al.,

153 2017).

154 2.2. Endocrine and Toxicological effects

155 Due to the extensive usage of the BP analogues and their widespread presence in

156 environment, many researchers have studied their toxic effects on human and animals

157 health. The most data is concerned the negative effects of BPA. It has been proven that

158 BPA is not only an endocrine disrupting chemical but also cause damage to hepatocytes

159 by oxidative stress. Moreover, it is supposed that BPA can modulate the immune

160 activity, contribute to obesity development and show mutagenic activity on eukaryotic

161 cells (Michałowicz, 2014). Early life BPA exposure lead to increased susceptibility to

162 mammary and prostate cancers (Seachrist et al., 2016). In addition, BPA disrupts

163 centrosome function and microtubule organization, displaying the broadest spectrum of

164 cancer-promoting effects (Ho et al., 2017). It has been reported to be particularly harmful

165 to the fetus, infants, and young children, because of lack of feedback regulating the

166 activity, synthesis, and elimination of hormone (Rykowska and Wasiak, 2006; Braun et

167 al., 2009). BPA exposure in childhood was associated with higher levels of inattention,

168 anxiety, hyperactivity, depression and conduct problems (Ejaredar et al., 2017). For more

169 details regarding toxic impact of BPA on vertebrates we refer the reader to the other

170 reviews (Rochester, 2013; Michałowicz, 2014; Seachrist et al., 2016).

171 BPAF was found to be more toxic to aquatic organisms Daphnia magna, Danio rerio

172 as well as Desmodesmus subspicatus, and to rats, than BPA (Stout, 2008; Tišler et al.,

173 2016). Given orally to these rodents, BPAF was accumulated in serum and various

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174 tissues with the highest concentrations detected in kidneys, liver, and adipose tissue

175 (Yang et al., 2012). BPAF acting at concentrations ≥ 10 nM as agonists and at

176 concentrations ≤ 10 nM as antagonists for estrogen receptors (ERα, ERβ), with effects

177 that are cell-dependent (Li et al., 2012). Furthermore, it bound more strongly to ER than

178 BPA what could cause adverse reproductive and developmental effects in several

179 different in vivo and in vitro models (Ruan et al., 2015). BPAF has been reported to

180 increase luteinizing hormone and follicle-stimulating hormone levels when was orally

181 administered to rats. Moreover, BPAF exposure caused dramatic decline in genes and

182 protein involved in cholesterol biosynthesis as well as transport and steroid biosynthesis

183 what resulted in inhibition of testosterone production (Feng et al., 2012). Increasing in

184 human erythrocytes level of cytosolic calcium and both calpain and caspase-3 activities

185 was also observed. In addition, BPAF exhibits eryptotic potential enabling the removal

186 of erythrocytes from circulation (Maćczak et al., 2016) and neurotoxicity. The latter is

187 caused through the disruption of microglial activation as well as cell death of neuronal

188 cells and mediated by calcium influx, generation of reactive oxygen species, activation

189 of extracellular signal regulated kinase: p38 and c-Jun N-terminal kinase, and caspase 3

190 (Lee et al., 2013a).

191 BPAP together with BPB, and BPZ were more estrogenic than BPA in human breast

192 cancer cells, whereas with BPM and BPP exhibited greater genotoxic potentials than that

193 of BPA in mutant chicken DT40 cells (Lee et al., 2013b; Mesnage et al., 2017).

194 Interestingly, this BPA analogue is capable of causing androgen receptor down-

195 regulation in castrate-resistant prostate cancers resulting in cell cycle arrest and

196 metabolic defects what may be a therapeutic strategy for prostate cancer patients (Stossi

197 et al., 2016).

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198 BPB is used in the manufacture of phenolic and polycarbonate resins. It is a potent

199 endocrine disruptor characterized with high estrogenic and anti-androgenic activities

200 (Kitamura et al., 2005; Yoshihara et al., 2004). Some authors suggested that BPB has

201 even stronger endocrine disruption potential than BPA. It was demonstrated that BPB

202 negatively influence on reproductive performance, gonadal development, sex hormones,

203 and the gene regulations in the hypothalamic-pituitary-gonadal axis of D. rerio (Yang et

204 al., 2017). Due to chemical similarity, it is assuming that BPA and BPB can

205 synergistically act with the same receptor sites (Grumetto et al., 2008). BPB was found

206 in canned fruits, vegetables, seafood and beverages from the Italian and Portuguese

207 markets (Grumetto et al., 2008; Cunha and Fernandes., 2010; Cunha et al., 2012; Cunha

208 and Fernandes, 2013). In addition, it was detected in human urine sample and its

209 presence in women’s serum was strongly linked with occurrence of endometriosis

210 (Cobellis et al., 2009; Cunha and Fernandes, 2010).

211 In humans, BPF has been detected in urine at concentrations and frequencies

212 comparable to BPA (Zhou et al., 2014). In vitro studies showed that it was cytotoxic,

213 genotoxic, estrogenic, and androgenic (Audebert et al., 2011; Molina-Molina et al.,

214 2013). Moreover, this BP showed other in vitro effects such DNA damage,

215 chromosomal aberrations and cellular dysfunction (Nakagawa and Tayama, 2000;

216 Cabaton et al., 2009; Pisapia et al., 2012; Lee et al., 2013a; Eladak et al., 2015). Rats

217 administered BPF via oral gavage had increased thyroid weight and altered thyroid

218 hormone concentrations. Changes to hematological parameters and enzyme expression

219 were also observed (Higashihara et al., 2007). However, no association between

220 exposure to BPF with thyroid nodular disease and thyroid hormones in human was

221 observed (Andrianou et al., 2016). In addition, the potential adverse effects of BPF and

222 BPS in the brain of mammals was observed. BPF and BPS affected 5α-reductase, a key

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223 enzyme involved in neurosteroidogenesis, as well as on dopamine- and serotonin-

224 related genes, in the prefrontal cortex of juvenile female rats (Castro et al., 2015).

225 Studies on BPS exposure in D. rerio revealed that BPS interfere with early-life

226 development. Low levels of BPS exposure increased both levels of GnRH endocrine

227 neurons which synthesized GnRH3 isoform controlling puberty, fertility and expression

228 of reproductive neuroendocrine-related genes (kiss1, gnrh3, erα). It may lead to

229 premature puberty and disorders of the reproductive system. Moreover, it was revealed

230 that thyroid hormone receptors partly mediate the stimulatory actions of BPS and BPA

231 on the reproductive neuroendocrine system. The authors highlighted that BPA-free

232 plastic products are not necessarily safer than products containing BPA (Qiu et al.,

233 2016). Another study in D. rerio showed that BPS exposure increased female to male

234 sex ratio, decreased body length, altered testosterone, estradiol, and vitellogenin

235 concentrations. In addition, decreased egg production, increased time to hatch,

236 decreased sperm count were also observed (Naderi et al., 2014). A sharp increase in

237 embryonic lethality and a corresponding decrease in fertility in the nematode C. elegans

238 was demonstrated by Chen et al. (2016). BPS elicits a stronger reproductive and DNA

239 damage repair gene response than BPA. The both BPs strong down-regulated msp-50

240 and msp-152 genes, implicated in the control of oocyte maturation and embryonic

241 viability. The suppression of msp-50 and msp-152 expression following BPS and BPA

242 exposure may play a significant role in impairing chromosome morphogenesis in

243 diakinesis. Furthermore, BPS even in fentomolar to picomolar concentrations can

244 induce rapid nongenomic signaling affecting the healthy functions of estrogen-

245 responsive pituitary cells. Moreover, it disrupts membrane-initiated estrogen estradiol

246 signaling that leading to altered cell proliferation, cell death, and prolactin release

247 (Viñas and Watson, 2013). It is suggested that BPS may affects adipogenesis as it is

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248 able to induce lipid accumulation and differentiation in primary human preadipocytes.

249 This effect may be mediated via direct activation of the nuclear receptor peroxisome

250 proliferator-activated receptor-γ (PPARG). BPS could also increase human adipocyte

251 protein 2 (aP2) promoter activity only in the presence of both PPARG and the

252 glucocorticoid receptor (Boucher et al., 2016). In addition, BPS like BPA demonstrate

253 the broadest spectrum of cancer-promoting effects as a results of disrupting centrosome

254 function and microtubule organization (Ho et al., 2017).

255 BPS possesses endocrine disruptive potencies (Molina-Molina et al., 2013; Cano-

256 Nicolau et al., 2016) while, it is predicted that its metabolites would show a lower

257 estrogenic activity. It results from in silico predictions of liver cytochrome-mediated

258 metabolism of BPS which identified specific 3-hydroxy-BPS and 2-hydroxy-BPS as its

259 metabolites. These compounds are structurally similar to 3-hydroxy-BPA and 2,2-Bis-

260 (4-hydroxyphenyl)-1-propanol, a BPA metabolites which showed a decreased

261 estrogenic activity with respect to BPA when tested in mammalian cell lines (Kitamura,

262 2005; Grignard et al., 2012).

263 BPP exhibit no estrogenic activity but showed genotoxic potentials involving DNA

264 double-strand breaks greater than BPA (Ike et al., 2002; Fic et al., 2013; Sangwoo Lee

265 et al., 2013; Chen et al., 2016). BPP demonstrated a high acute toxicity against D.

266 magna, since the 48-h EC50 was 1.6 mg L-1, whereas EC50 values of BPA was 10 mg L-1

267 (Chen et al., 2002). The 6-h LC50 against 24-h-old larva medaka (Oryzias latipes) was

268 2.3 mg L-1 and was about 6-fold higher than that of BPA (Yokota et al., 2008).

269 BPZ is one of the least well known BPs. So far, its difference in potency between the

270 estrogen receptors ERα and ERβ was notable. Comparable to BPAF, BPAP, BPB, BPZ

271 exhibited higher affinity for ERβ than that for ERα. It acts as ERβ antagonists, while on

272 ERα it acts largely as agonists or mixed agonists and antagonists (Stossi et al., 2016).

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273 3. Biodegradation of bisphenols in aquatic environment

274 Due to the ubiquitous occurrence of bisphenols in aquatic systems (Tišler et al., 2016),

275 it is urgent need to understand their fate in this environment. BPs undergo chemical and

276 biological processes, among which biodegradation seems to be the major removal

277 mechanisms (He et al., 2010). Biodegradation resulted from the use of BPs by some

278 bacteria as sole and energy sources, while growth of other strains is inhibited by these

279 compounds (Kolvenbach et al., 2014). However, the knowledge about the mechanism of

280 toxicity of BPs on bacterial cells is limited and applies only to BPA. This compound has

281 strong antibacterial activity against Staphylococcus aureus, Bacillus subtilis, Proteus

282 vulgaris and Escherichia coli. The authors suggested that BPA may blocks lipid

283 synthesis, intercalate into bacterial cell membranes and disrupt membrane activities

284 without causing leakage of intracellular components (Rasheed et al., 2013). No data are

285 available on the toxicity of BPA on the entire bacterial community. Nevertheless, it can

286 be assumed that BPA may affects on bacterial population in a similar way as triclosan

287 does. It is an chlorinated diphenol widely distributed in WWTP and rivers, which

288 disturbs bacterial community due to the inhibition of synthesis of cell wall fatty acid

289 (Ricart et al., 2010).

290 Bacteria can utilize the full space of catabolic biochemical reaction types to initiate

291 biodegradation. Biodegradation of BPs has been mostly studied with BPA. Until now,

292 two main BPA biodegradation mechanisms have been identified (Fig. 1). The first

293 involves the oxidative skeletal rearrangement of an aliphatic methyl group in the BPA

294 molecule. It has been shown for Sphingomonas sp. MV1 (Lobos et al., 1992; Spivacks

295 et al., 1994) Sphingomonas sp. AO1 (Sasaki et al., 2005), Sphingomonas sp. BP-7

296 (Sakai et al., 2007), Cupravidus basilensis JF1 (Fischer et al., 2010) and

297 Novosphingobium sp. TYA-1 (Toyama et al., 2009). For BPA biodegradation by strain

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298 MV1 major (Fig. 1, a) and minor (Fig. 1, b) pathways have been revealed. In the major

299 pathway, as a result of hydroxylation of the quaternary carbon of BPA, 1,2-bis(4-

300 hydroxyphenyl)-2-propanol (compound I) is formed. Compound I is dehydrated to 4,4’-

301 dihydroxy-methylstilbene (compound II) followed by oxidative cleavage to form 4-

302 hydroxyacetophenone (HAP) and 4-hydroxybenzaldehyde (HBAL). The latter is

303 oxidized to 4-hydroxybenzoic acid (HBA). Both HAP and HBA are further mineralized

304 as no other compound were detected by HPLC-UV analysis. In the minor pathway,

305 BPA is metabolized to 2,2-bis(4-hydroxyphenyl)-1-propanol (compound III) by the

306 hydroxylation of methyl group. Compound III is simultaneously oxidized and

307 rearrangement to form 2,3-bis(4-hydroxyphenyl)-1,2-propanediol (compound V) further

308 slowly degraded to HBA and 4-hydroxyphenacyl alcohol (compound VI). Compound

309 III is also metabolized a much lesser extent to 2,2-bis(4-hydroxyphenyl)propanoic acid

310 (compound IV). Strain Sphingomonas sp. MV1 is able to biotransform also BPB, bis(4-

311 hydroxyphenyl)diphenylmethane [BPBP], 2,2-bis(4-hydroxy-3-methylphenyl) [BPC],

312 bis(4-hydroxy-phenyl)ethane [BPE], 2,2-bis(4-methoxyphenyl)propane [BPC], 1,1-

313 bis(4-hydroxyphenyl)cyclopentane, 3,3-bis(4-hydroxyphenyl)pentane and trans-4,4'-

314 dihydroxystilbene (Lobos et al., 1992; Spivacks et al., 1994). Other metabolic

315 degradation of BPA is used by C. basilensis JF1 (Fig. 1, c). BPA is cleaved into 4-(2-

316 propanol)-phenol (compound VII) and p-hydrochinone (compound VIII) which is

317 followed by mineralization. 4-(2-propanol)-phenol is mainly dehydrated to form 4-

318 isopopenylphenol (compound IX). The other intermediate HAP which is poorly used for

319 growth is formed after splitting of a C1-body from compound VII. Compound IX is

320 oxidized to HBAL which subsequent with HAP is further degraded via ortho-

321 degradation pathway (Fischer et al., 2010).

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322 The second BPA degradation pathway involves hydroxylation of one or two phenolic

323 rings following by aromatic ring cleavage and it was demonstrated for S. fuliginis OMI

324 (Fig. 1, d). Among this pathway, two possible BPA biotransformation models were

325 distinguished. In first model, 3-hydroxy BPA (compound X) is formed after the

326 hydroxylation of the one of the BPA phenolic rings. Thereafter, both aromatic rings

327 from compound X are hydroxylated to generate compound XI. It is also possible that

328 phenolic rings from BPA are directly hydroxylated to metabolite XI (Fig. 1, e). Further,

329 one of the rings is cleaved at meta position to form compound XII followed by

330 degradation to product XIII.

331

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333

334 Figure 1. Proposed biodegradation pathways of BPA by Spingomonas sp. MV1 (a, b), C. basilensis JF1 (c) and S. fuliginis OMI (d, e). The
335 names of compounds are given in the text. The alternatives pathways are indicated by dashed arrows

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336 In the second model, the aromatic ring from compound X is cleaved at the meta position

337 (compound XIV) followed by further degradation into metabolite XV. Intermediate

338 XIV may be also hydroxylated to generate compound XII. Metabolites XV and XII are

339 degraded to product XIII (Ogata et al., 2013).

340 Another bisphenol, which metabolic pathway of degradation was identified is BPF.

341 This pathway in detail was described for Sphingobium yanoikuyae FM-2 (Figure 2).

342 Bis(4-hydroxyphenyl)methanol (compound I) is formed after hydroxylation of the BPF

343 bridging carbon and further is oxidized to 4,4`-dihydroxybenzophenone (compound II).

344 Subsequently, the Baeyer-Villiger reaction take place: an oxygen atom is inserted

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345 between the carbon atoms of the ketone group and one of the phenolic rings in

346 compound II. The formed 4-hydroxyphenyl 4-hydroxybenzoate (compound III) is

347 oxidized to 4-hydroxybenzoate (compound IV) and 1,4-hydroquinone (compound V).

348 Metabolite IV is directly mineralized, while some compound V is mineralized, and

349 some portion is subjected to reversible auto-oxidation to 1,4-benzoquinone (compound

350 VI) (Inoue et al., 2008). The degradation pathway of BPF by Sphingobium yanoikuyae

351 TYF-1, isolated from P. australis rhizosphere, seems to be partly similar to that

352 proposed for strain FM-2 and involves oxidations as key step (Toyama et al., 2009).

353

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354

355

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358

359

360

361

362

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364

365

366

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370 Figure 2. Proposed pathway for BPF biodegradation by S. yanoikuyae FM-2

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378 Detailed pathways of biological decomposition of other bisphenols are not known.

379 Nevertheless, Zühlke et al., (2016) demonstrated that BPA, BPF, BPC (2,2-bis-(4-

380 hydroxy-3-methylphenyl)-propane) and BPE were converted by Bacillus

381 amyloliquefaciens isolated from activated sludge of a municipal sewage treatment plant

382 to less toxic and less estrogenically active phosphate conjugates. In labor studies mainly

383 the potential of single bacterial strains to BPA degradation were determined (Spivack et

384 al., 1994; Sakai et al., 2007; Yamanaka et al., 2008; Matsumura et al., 2009; Saiyood et

385 al., 2010).

386 Due to fact that in many ecosystems microorganisms form species-rich communities

387 that are able to degrade a wider range of substrates than the isolated degrader alone,

388 research on such assemblage are ecologically relevant. Nevertheless, a knowledge about

389 BPA and other BPs biodegradation by bacterial consortia is limited. It is believed that

390 BPA in seawater is degraded by microbial consortia by a synergistic action. So far, few

391 strains capable of degrading BPA and some other BPs have been isolated from this

392 nutrient-poor environment. One of these bacteria is Sphingomonas sp. BP-7 which alone

393 degraded of 100 ppm BPA within 40 days. Interestingly, when the BPA degradation

394 was enhanced by other strains isolated from seawater: Pseudomonas sp. BP-14,

395 Pseudomonas sp. BP-15, and strain no. 24A, the degradation took only 7 days.

396 Pseudomonas strains did not degrade BPA, but support the growth of Sphingomonas sp.

397 BP-7. In addition, the latter was able to decompose BPC, BPE, BPZ and BPB, however

398 it did not degrade BPS (Sakai et al., 2007). The impact of bacterial community collected

399 from seawater on BPA, BPF and BPS biodegradation was studied by Danzl et al.

400 (2009). Samples lacking microorganisms were applied as controls. The authors

401 demonstrated that BPA and BPF were only degraded in the water with microbial

402 community indicating that the biodegradation of the BPs is connected with catabolic

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403 activity of bacteria. BPS was not degraded, thus it is more likely to accumulate in the

404 aquatic environment (Danzl et al., 2009). So far, Sphingobium fuliginis OMI is the only

405 identified strain that has the ability to decompose BPS (Ogata et al., 2013).

406 Interestingly, it has been shown that bacteria exhibiting the rhizosphere of aquatic plant

407 Phragmites australis enhance degradation of BPA and BPF. This process may be

408 stimulated by the releasing of oxygen by plants to soil surroundings the root system

409 (Toyama et al., 2009). Most of researches described the BPA degradation by bacteria

410 consortia in WWTP and rivers, therefore they will be discussed in the following

411 subsections.

412 3.1. Biodegradation of BPA by bacterial communities in WWTP

413 Bacteria play a key role in detoxification of BPA-containing wastewaters. Despite the

414 fact that in effluent BPA content is over 90% lower than in influent, it can be a source of

415 this pollution in the aquatic environment (Kang et al., 2006). The most commonly used

416 technology for biological wastewater treatment is the activated sludge process. It

417 depends heavily on the metabolism and interactions of the microbial community as

418 bacteria play a major role in the purification process as they are responsible for both

419 nutrients and xenobiotics removal (Hashimoto et al., 2014). The activated sludge, is a

420 highly species-rich ecosystem comparable to soil (Ye and Zhang, 2013). It was revealed

421 that Betaproteobacteria was the most abundant class in the phylum of Proteobacteria,

422 followed by Gammaproteobacteria (Kwon et al., 2010; Snaidr et al., 1997). Otherwise,

423 Ye and Zhang (2013) reported that Alphaproteobacteria and Actinobacteria were the top

424 two classes in the activated sample. The bacterial community structures changed

425 depending on the chemical compounds presence in the wastewater.

426 It was demonstrated that bacterial consortia from activated sludges were capable of

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427 complete degradation of BPA for concentrations up to 50 mg L−1 in light and dark

428 incubations to intermediates, further degraded to harmless end products (Eio et al.,

429 2014). These consortia contain both BPA- and non-BPA-degraders which cooperate with

430 each other. Microorganisms incapable of BPA degradation, can help in the removal of

431 this chemical through enhancement of either the activity of BPA-degraders or through

432 co-metabolism (Chong and Lin, 2007; Zhao et al., 2014).

433 One of the group of microorganisms involved in co-metabolism of BPA are

434 ammonium-oxidizing bacteria (AOB) that expressed ammonia monooxygenase (AMO)

435 enzyme. Aside from oxidize of ammonia, AMO enzyme catalyzed an oxidation of wide

436 range of aromatic and aliphatic hydrocarbons (Keener and Arp, 1994). Already presented

437 data reported that nitrifying activated sludges as well as pure culture of an ammonia

438 oxidizer - Nitrosomonas europaea removed natural and synthetic estrogens with the

439 same activity as BPA (Vader et al., 2000; Shi et al., 2004; Yi and Harper, 2007). Vader

440 et al. (2000) as the first have reported that nitrifying sludges in volume 15 ml where the

441 initial cell density was 1.0 g L-1 degraded the synthetic steroid 17-α-ethinylestradiol

442 (EE2) at the initial concentration of 50 μg L-1 completely within six days. The

443 degradation is mediated by AMO activity, what proved the significant role of AMO in

444 the BPA detoxification processes. When allylthiourea (ATU), an AMO inhibitor was

445 added to the nitrifying activated sludges, degradation of EE2 decreased by 40% over 56 h

446 while its addition to pure culture of N. europaea completely inhibited removal of natural

447 estrogen. Co-metabolic degradation of EE2 by AOB was also suggested by Yi and Harper

448 (2007). A linear relationship between nitrification and EE2 biodegradation rates was

449 reported. Both of these processes did not occur in the presence of ATU. Moreover,

450 during the EE2 biodegradation, OH-EE2 appeared as a metabolite what is characteristic

451 for monooxygenase activity. The authors shown that the heterotrophic bacteria did not

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452 promote EE2 removal and concluded that autotrophs are the key players in this process

453 (Yi and Harper, 2007). However, nitrifies can initially degrade EE2 into intermediates

454 which then may serve as a substrate for heterotrophic microorganisms. In the activated

455 sludge processes are many fast-growing heterotrophs that have a variety of mono- and

456 dioxygenase enzymes. These cultures may contribute to or even dominate

457 micropollutants biotransformation. An indication for that is the degradation of

458 intermediates in mixed cultures which otherwise would be present in pure AOB cultures

459 (Shi et al., 2004; Yi and Harper, 2007; Skotnicka-Pitak et al., 2009). Gaulke et al. (2008)

460 claimed that EE2 degradation at low concentration running in the municipal treatment

461 activated sludges system is presumably due to the activity of heterotrophic

462 microorganisms and not due to the co-metabolism of AOB. The authors emphasize the

463 importance of the conditions of the artificial environment created in batch test as in the

464 previous bench-scale studies the estrogen concentration were much higher than those in

465 WWTP influents as well as the initial ammonium nitrogen. It has been shown that

466 compounds present at low concentrations (µg/L range or lower) may show quite different

467 biodegradation pattern than they occurs at high concentrations (mg/L range). In addition,

468 biodegradation is preferred when chemicals are presented at low concentrations and then

469 co-metabolism may predominate (Skotnicka-Pitak et al., 2009; Khunjar et al., 2011).

470 To assess the relative contribution of AOB and heterotrophs in EE2 biotransformation,

471 Khunjar et al. (2011) conducted experiments using pure AOB, mixed culture containing

472 nitrifies and heterotrophs and two heterotrophic cultures devoid of nitrifies activity. The

473 heterotrophic cultures were grown in chemostats and fed acetate, benzoate and toluene to

474 obtain enriched oxygenase activity or only with acetate to generate minimal oxygenase

475 activity. The results revealed that AOB were able to biotransformation but not

476 mineralization of EE2 under ammonia-limited but AMO-rich growth conditions. The

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477 validity of AOB was confirmed as the bacteria degraded EE2 even at low concentration

478 (ng/L). In addition, AOB removed EE2 five times faster than heterotrophic

479 microorganisms, however, heterotrophs degraded EE2 independent of AOB activity.

480 AOB biotransformed EE2 to hydroxyl- EE2 and sulfo- EE2, among which the former was

481 further biotransformed by heterotrophic organisms. Moreover, heterotrophs biodegraded

482 2-nitro- EE2 and 4-nitro- EE2 which were abiotically generated in AOBs culture.

483 Recent findings have shown that the diversity and biomass of AOB communities

484 decreased after exposure to BPA. Sequencing of selected bands from gel and

485 phylogenetic analysis showed that AOB belonged to the genus Nitrosospira, among

486 which N. briensis showed the highest tolerance to BPA. Interestingly, the authors

487 suggest that contribution AOB to BPA degradation was limited as the nitrification

488 efficiency was not correlated with BPA removal, whereas this process was related with

489 activity of heterotrophs, which were resistant to BPA exposure (Zielińska et al., 2014).

490 Moreover, the AOB diversity was reduced when increasing organic compounds were

491 loading. These chemicals in the wastewater favor fast-growing bacteria that dominate

492 slower-growing species (Xia et al., 2008).

493 An alternative to activated sludges in efficient wastewater treatment are aerobic

494 granules which are aggregates with functional strains that are embedded in EPS,

495 inorganic compounds and various minerals (Adav et al., 2008). Studies on the microbial

496 structure of granules exposed to BPA have been performed by Cydzik-Kwiatkowska et

497 al. (2017). The results indicated that addition of BPA to the reactors decreased the

498 microbial diversity. The most abundance phyla were Proteobacteria, Bacteroidetes and

499 Verrucomicrobia. The predominant Proteobacteria was Betaproteobacteria. The

500 increasing BPA influent concentrations caused increase in abundance of

501 Alphaproteobacteria as well as Burkholderiales, Methylophilales and Methylococcales

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502 families. The most numerous family in the biomass was Rhodocyclaceae. In contrast,

503 Pseudomonadales were sensitive to the presence of BPA in influent. The abundance of

504 the genera Sphingomonas, Sphingopyxis, Pusillimonas, Methylobacillus, Methylomonas

505 and Nitrosospira in opposite to Thauera and Aquimonas significantly correlated with

506 BPA influent concentrations. The authors stressed that in mixed microbial consortia, the

507 BPA removal cannot be directly linked with the microbial structure of biomass as the

508 presence of some microorganisms in biomass is not equivalent to the fact that they are

509 BPA-degraders.

510 3.2. Degradation of BPA by bacterial communities in rivers

511 Rivers are important to society, providing water for consumption, agriculture and

512 carrying away wastes. Planktonic as well as attached bacteria populations in rivers, play

513 an important role in the biodegradation of pollutants derived from human activities. This

514 might allow to profitable and essential improvement in water quality (Cai et al., 2016).

515 Bacterial biodegradation seems to be a key factors in the elimination of BPA in rivers,

516 thus restrict the potential risk of BPA (Yang et al., 2014). Although, in rivers are many

517 bacteria able to remove BPA, those with high BPA biodegradability are limited. It was

518 demonstrated that bacteria isolated from 40 out of 44 samples from different site of

519 seven rivers could biotransformed this compound to different intermediates, among

520 which bacteria only from 6 samples were capable of complete BPA biodegradation

521 (Kang et al., 2006). The results obtained by Kang and Kondo (2002a) showed that 91%

522 of bacteria isolated from three rivers were able to BPA removal with different

523 effectiveness (18-91%) of which, the increased ability to remove BPA had only two

524 strains: Pseudomonas putida and Pseudomonas sp. Noteworthy, greater number of

525 bacteria and higher temperatures favored the degradation of BPA (Kang and Kondo,

526 2002b). However, some authors did not observe correlations between bacterial counts

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527 and BPA degradation (Klecka et al., 2001). This discrepancy may arise due to the

528 bacterial population size that can do fastly and completely remove BPA (Kang et al.,

529 2006). Moreover, the availability of oxygen influence removal of BPA. It was well

530 documented, that BPA under aerobic condition was rapidly biodegraded (> 90%), while

531 the efficiency of this process was significantly reduced (< 10%) in the absence of oxygen

532 (Kang and Kondo, 2002b).

533 Bacteria inhabiting sediments of the rivers are also capable of degradation of organic

534 pollutants including BPs. However, degradation rate is influenced by many

535 environmental factors such as pH, content of dissolved oxygen, dissolved organic

536 carbon, inorganic nutrients, stoichiometric ratios of nutrients and BPA amounts (Cai et

537 al., 2016). The composition of bacterial community associated with BPA degradation

538 from Wenyu River sediment (China) revealed that the predominant bacterial groups were

539 Gammaproteobacteria and Alphaproteobacteria (Yang et al., 2014), whereas from

540 surface sediment from a river in an electronic waste dismantling zone in Guangdong

541 Province (China) Betaproteobacteria, Alphaproteobacteria, and Gammaproteobacteria

542 (Xiong et al., 2017a). Many bacteria from Alphaproteobacteria are able to produce EPS

543 providing a protective conditions for cells to grow and persist. Betaproteobacteria

544 dominated the sediment whereas Gammaproteobacteria was linked to the removal of

545 phenolic compounds (Douterelo et al., 2013; Yang et al., 2015). The BPA-degrading

546 bacterial communities of sediment from Beiyun Canal (China) were mainly composed of

547 Proteobacteria, Bacteroidetes, Chloroflexi, Firmicutes, Gemmatimonadetes, and

548 Actinobacteria. However, the bacterial composition changed with incubation time (Yang

549 et al., 2015). In another experiment, Huang et al. (2017) analyzed the variation of

550 bacterial communities in sediment from Xiangjiang River (China). They concluded that

551 BPA significantly affected the abundance and diversity of bacteria. The changes in the

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552 taxonomic composition of bacterial community under BPA exposure supported BPA

553 biodegradation by promoting the growth of bacteria from Pseudomonas and

554 Sphingomonas genus identified as BPA-reducing bacteria. The strains presented over

555 73% of the original bacterial community. Aneurinibacillus aneurinilyticus,

556 Symbiobacterium and Firmicutes which BPA biodegradation ability have rarely been

557 reported were inhibited by BPA during the period of incubation. The analysis of bacterial

558 groups involved in BPA degradation within natural biofilms in Qinhuai River (China)

559 revealed that contribution of Burkholderiaceae, Sphingomonadacea and

560 Pseudomonadaceae to total bacterial community were positively related to higher BPA

561 concentration, whereas Comamonadaceae, Alcaligenaceae and Rhizobiaceae

562 demonstrated negative correlation with the BPA content (Cai et al., 2016). The results

563 obtained by Peng et al. (2015) showed that the degradation ability of two mixed strains

564 was higher than that of single isolate but much weaker than that of microbial consortium.

565 The authors concluded that BPA degradation may have been enhanced by bacterial

566 communities due to the cooperation in BPA and toxic intermediates removal as well as

567 the support in the metabolism of the degraders.

568 A three-year study conducted by Guo et al., (2016) added information about bacterial

569 groups in Daling River (China) sediment exposed to paper mill pollution (PMP),

570 including chlorinated BPA. The Clostridia and Epsilonproteobacteria at the class level,

571 and Fusibacter and Desulfobulbus at the genus levels were selected as an indicators of

572 PMP. Clostridia are able to survive under unfavorable conditions in aquatic

573 environments in the sporing stage, while the presence of Epsilonproteobacteria is

574 correlated with sulphur cycles. The high abundance of Fusibacter and Desulfobulbus

575 may have been a result of a the high concentration of total polychlorinated biphenyl

576 content (Papapetropoulou, 1997; Guo et al., 2016).

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577 4. Conclusion

578 In the face of the increasing usage of bisphenol analogues and their human and

579 ecological hazard effects, there is an urgent need to know their fate in the environment.

580 Until now, the presence of BPAF, BPAP, BPB, BPF, BPP, BPS, and BPZ have been

581 detected e.g. in WWTP, dust, surface waters, sediments and soil. Among these

582 environments, bacteria capable of bisphenols degradation have been found. However, the

583 great majority studies focused on isolation a single bacterial strains while degradation of

584 organic pollutants is a cooperative process with the participation of various microbes.

585 Few of the research investigated participation and/or composition of these communities

586 in WWTP and rivers as well as characteristics of their BPs biodegradation pathways. In

587 summary, the existing data about bacterial community in BPs biodegradation are very

588 limited. Moreover, the assessment of the impact of BPA analogues on human and

589 wildlife is not sufficient. Future research is needed to better elucidate their environmental

590 occurrence and persistence. Especially studies addressing microbial degradation by

591 bacterial communities to identify environmental transformation products and fate of

592 bisphenols should be conducted.

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951

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Highlights
 Occurrence of bisphenols in environment
 Toxicity of bisphenols
 The pathways of BPA and BPF biodegradation
 The biodegradation of bisphenol A by bacterial consortia