Suitability of Immobilized Systems for Microbiological Degradation of Endocrine Disrupting Compounds

<a href="/goto?url=http://www.mdpi.com/journal/molecules" target="_blank">molecules </a>Review Suitability of Immobilized Systems for Microbiological Degradation of Endocrine Disrupting Compounds Danuta Wojcieszyn´ska , Ariel Marchlewicz and Urszula Guzik * Institute of Biology, Biotechnology and Environmental Protection, Faculty of Natural Science, University of Silesia in Katowice, Jagiellon´ska 28, 40-032 Katowice, Poland; [email protected] (D.W.); [email protected] (A.M.) * Correspondence: [email protected]; Tel.: +48-3220-095-67 Academic Editors: Urszula Guzik and Danuta Wojcieszyn´ska Received: 10 September 2020; Accepted: 25 September 2020; Published: 29 September 2020 <a href="/goto?url=http://www.mdpi.com/1420-3049/25/19/4473?type=check_update&version=1" target="_blank">ꢀꢁꢂꢀꢃꢄꢅꢆꢇ </a><a href="/goto?url=http://www.mdpi.com/1420-3049/25/19/4473?type=check_update&version=1" target="_blank">ꢀꢁꢂꢃꢄꢅꢆ </a>Abstract: The rising pollution of the environment with endocrine disrupting compounds has increased interest in searching for new, effective bioremediation methods. Particular attention is paid to the search for microorganisms with high degradation potential and the possibility of their use in the degradation of endocrine disrupting compounds. Increasingly, immobilized microorganisms or enzymes are used in biodegradation systems. This review presents the main sources of endocrine disrupting compounds and identifies the risks associated with their presence in the environment. The main pathways of degradation of these compounds by microorganisms are also presented. The last part is devoted to an overview of the immobilization methods used for the purposes of enabling the use of biocatalysts in environmental bioremediation. Keywords: EDCs; hormones; degradation; immobilization; microorganisms 1. Introduction The development of modern tools for the separation and identification of chemical substances has drawn attention to the so-called micropollution of the environment. Many of these contaminants belong to the emergent pollutants class. According to the Stockholm Convention they are characterized by high persistence, are transported over long distances in the environment through water, accumulate in the tissue of living organisms and can adversely affect them [ include pharmaceuticals, the presence of which are not only found in hospital or municipal sewage but also in Arctic water or drinking water [ ]. In many laboratories, new methods for the degradation 1]. Substances meeting these criteria 1,2 of these compounds are being developed, with the use of microorganisms that have an increased potential for the degradation of these compounds. Biological treatment is a promising technology due to its low cost and reduced energy requirements [ these microorganisms in the complex microbial consortia of wastewater treatment plants [ more and more attention has been paid to immobilized systems, in which these strains are protected by binding them to a carrier [ ]. The use of microorganism immobilization in the drug’s biodegradation <ul style="display: flex;"><li style="flex:1">3</li><li style="flex:1">,4 </li></ul>]. However, the main problem is the survival of 5]. Hence, <ul style="display: flex;"><li style="flex:1">4</li><li style="flex:1">,6,7 </li></ul>not only protects them from harmful environmental conditions, but also leads to an increase in the intensity of the biotransformation processes as a result of the local thickening of the biomass and a higher tolerance of the bacterial cells to these pharmaceuticals [ 4,7]. The intensive development of immobilization methods has led to the discovery of many carriers and immobilization techniques [ <ul style="display: flex;"><li style="flex:1">7</li><li style="flex:1">,8 </li></ul>]. The new techniques differ in the level of difficulty of the procedure used, cost-effectiveness, efficiency of the processes carried out in the immobilized systems and the usefulness in the immobilization of the microorganisms. For this reason, the purpose of this work is to review the achievements to date in the <ul style="display: flex;"><li style="flex:1">Molecules 2020, 25, 4473; doi:<a href="/goto?url=http://dx.doi.org/10.3390/molecules25194473" target="_blank">10.3390</a><a href="/goto?url=http://dx.doi.org/10.3390/molecules25194473" target="_blank">/</a><a href="/goto?url=http://dx.doi.org/10.3390/molecules25194473" target="_blank">molecules25194473 </a></li><li style="flex:1"><a href="/goto?url=http://www.mdpi.com/journal/molecules" target="_blank">ww</a><a href="/goto?url=http://www.mdpi.com/journal/molecules" target="_blank">w</a><a href="/goto?url=http://www.mdpi.com/journal/molecules" target="_blank">.</a><a href="/goto?url=http://www.mdpi.com/journal/molecules" target="_blank">mdpi.com</a><a href="/goto?url=http://www.mdpi.com/journal/molecules" target="_blank">/</a><a href="/goto?url=http://www.mdpi.com/journal/molecules" target="_blank">journal</a><a href="/goto?url=http://www.mdpi.com/journal/molecules" target="_blank">/</a><a href="/goto?url=http://www.mdpi.com/journal/molecules" target="_blank">molecules </a></li></ul>Molecules 2020, 25, 4473 2 of 25 field of using immobilized systems in the endocrine disrupting compounds biodegradation processes. This will systematize the existing knowledge about the subject and indicate the advantages and disadvantages of the methods used, as well as the needs and perspectives for the further development of immobilization methods. 2. Endocrine Disrupting Compounds (EDCs) in the Environment and Associated Risks Endocrine disrupting compounds (EDCs) are natural or synthetic substances that, when introduced into the environment, affect the endocrine and homeostatic system of non-target organisms by disabling their communication and response to environmental stimuli. These include estrogens- natural and synthetic female and male hormones that play an important role in both the reproductive and the non-reproductive systems [ considered to be the strongest among the endocrine factors in the environment [10]. Synthetic estrogens have been divided into steroidal, such as 17 -ethynylestradiol and 3-methyl ether of ethynylestradiol, used as ingredients of birth control pills, and nonsteroidal estrogens such as diethylstilbestrol used to prevent miscarriages [ 11]. Human use of the latter was banned in 1972 due to its negative effects, 3,6,9]. Estrone, estriol and 17β-estradiol are natural estrogens. The latter is α3,7, however, it is still used in China as a growth promotor for terrestrial livestock or fish [11]. The presence of estrogens has been reported in many aquatic environments (Table 1). Table 1. Occurrence of EDCs in the environment. EDCs Estrone Concentration 10.4 ng/L <ul style="display: flex;"><li style="flex:1">Occurrence </li><li style="flex:1">Sampling Period </li></ul>Spring to autumn Spring to autumn Spring to autumn December to May December to May December to May May References [4] Leca River (Portugal) Leca River (Portugal) Leca River (Portugal) Wuluo River (Taiwan) Wuluo River (Taiwan) Wuluo River (Taiwan) 17β-Estradiol Estriol <ul style="display: flex;"><li style="flex:1">5.9 ng/L </li><li style="flex:1">[4] </li></ul><ul style="display: flex;"><li style="flex:1">4.4 ng/L </li><li style="flex:1">[4] </li></ul><ul style="display: flex;"><li style="flex:1">Estrone </li><li style="flex:1">1.27 ng/L </li><li style="flex:1">[12] </li></ul>[12] [12] [13] [13] [14] [14] [15] [16] [16] [17] [17] [18] 17β-Estradiol Estriol 313.60 ng/L 210.00 ng/L 40–117 ng/L 9.78–151 ng/L 0.076–0.233 ng/L 0.68 ng/L Surface water of Taihu Lake, China Sediments of Taihu Lake, China Lake Balaton, Hungary River Zala, Hungary Yangtze estuary, China Themi River, Tanzania Kalansanan River, Malaysia Fenholloway River, USA Fenholloway River, USA 17β-Estradiol 17β-Estradiol 17β-Estradiol May No data <ul style="display: flex;"><li style="flex:1">17α </li><li style="flex:1">-Ethynyl-estradiol </li></ul>Estrogen No data 3.22–20.61 ng/L 20.4–439 ng/L 16,689 ng/L 40 ng/L Four seasons <ul style="display: flex;"><li style="flex:1">March </li><li style="flex:1">Progesterone </li></ul><ul style="display: flex;"><li style="flex:1">Progesterone </li><li style="flex:1">No data </li></ul>Androstenedione Progesterone May and December May and December High rainy periods 2060 ng/L Atibaia River, Brazil 17α-Ethynyl-estradiol 981–4390 ng/L Molecules 2020, 25, 4473 3 of 25 Table 1. Cont. <ul style="display: flex;"><li style="flex:1">EDCs </li><li style="flex:1">Concentration </li></ul>17–501 ng/L <ul style="display: flex;"><li style="flex:1">Occurrence </li><li style="flex:1">Sampling Period </li></ul>Dry winter period High rainy periods Dry winter period References [18] Atibaia River, Brazil Atibaia River, Brazil Atibaia River, Brazil 17α-Ethynyl-estradiol <ul style="display: flex;"><li style="flex:1">17β-Estradiol </li><li style="flex:1">464–6806 ng/L </li></ul>106–2273 ng/L [18] <ul style="display: flex;"><li style="flex:1">17β-Estradiol </li><li style="flex:1">[18] </li></ul>High rainy periods and dry winter period Atibaia River, Brazil <ul style="display: flex;"><li style="flex:1">Estrone </li><li style="flex:1">16 ng/L </li><li style="flex:1">[18] </li></ul>Atibaia River, Brazil Atibaia River, Brazil Atibaia River, Brazil Atibaia River, Brazil Progesterone Progesterone Levonorgestrel Levonorgestrel 20 ng/L 20–195 ng/L 19 ng/L High rainy periods Dry winter period High rainy periods Dry winter period [18] [18] [18] <ul style="display: flex;"><li style="flex:1">[18] </li><li style="flex:1">19–663 ng/L </li></ul>High rainy periods and dry winter period Atibaia River, Brazil <ul style="display: flex;"><li style="flex:1">4-Octylphenol </li><li style="flex:1">21 ng/L </li><li style="flex:1">[18] </li></ul>High rainy periods and dry winter period Atibaia River, Brazil <ul style="display: flex;"><li style="flex:1">4-Nonylphenol </li><li style="flex:1">18 ng/L </li><li style="flex:1">[18] </li></ul>Testosterone Testosterone Estrogen Estrogen Estriol 1.9–2.7 ng/L 1.0–3.8 ng/L 0.6–2.2 ng/L 1.2–3.4 ng/L 0.9–1.8 ng/L 0.9–2.9 ng/L Lower Jordan River Lower Jordan River Lower Jordan River Lower Jordan River Lower Jordan River Lower Jordan River May October May October May October [19] [19] [19] [19] [19] <ul style="display: flex;"><li style="flex:1">[19] </li><li style="flex:1">Estriol </li></ul>One of the main sources of estrogens in a highly urbanized environment is urine and faeces getting into wastewater. It has been shown that annually 33 and 49 tonnes of estrogen excreted from farms in the European Union and the United States, respectively, are released into the environment [12,20]. In human and animal organisms, estrogens are usually hydroxylated or conjugated with glucuronide or sulfate hence these forms most often get into wastewater. It is estimated that about 90% of urine estrogens are in the form of conjugates. Most estrogen conjugates are more polar than parent molecules, so they can be more mobile in the environment. Despite the fact that conjugates have low estrogenic potential, they can be chemically or enzymatically hydrolysed to active forms in the environment. For example, the Escherichia coli strain KCTC 2571 has β-glucuronidase, which cleaves glucuronide moieties, releasing free estrogen [20,21]. As a result of the operation of sewage treatment plants, 19–94% of estrogens are biodegraded and biotransformed. Typically, concentrations in the range of 1–3 ng/L are observed in the effluents from treatment plants [3]. Although these compounds occur in the environment in concentrations of ng/L, it is known that they can have a strong negative impact in amounts below 1 ng/L because they have a high affinity for nuclear estrogen receptors. This biological activity can lead to low levels of estrogen in the environment causing endocrine disorders in the wildlife population. Negative effects on development, sex differentiation, reproduction of different animal species and production of vitellogenin have been documented [ negative impact on the sexual behaviour of frogs in suburban areas in the United States have been observed [12]. In addition, it has been shown that 17 -estradiol, at concentrations of 0.1–1 ng/L, causes 3,4,7,11,12]. Intersexual disorders in fish in Europe, and a βreproductive disorders in aquatic animals. Disrupting in the development, spawning and fertility of Japanese medaka (Oryzias latipes) was showed at low estrogen concentrations [20]. An increase in osteoblast activity was also detected in fish such as goldfish and wrasse, which resulted in the Molecules 2020, 25, 4473 4 of 25 mobilization and mineralization of fish scales [22]. The presence of this compound in the environment may cause disturbances in the secretion of endogenous gonadal sex hormone in humans and reduce sperm production, as well as increase the incidence of cancer [6]. In addition, it has been observed that often the response to estrogens is dependent on the age of the organisms. For instance, adults of common roach showed a slight response to the presence of estrogens, while exposure to hormonal compounds during the embryonic period caused 100% feminization in fish. In toxicological studies at various developmental stages, Atlantic salmon showed a higher level of vitellogenin mRNA in the presence of EDCs in all stages, except in embryos. In addition, embryos were only sensitive to the highest levels of 17α-ethynylestradiol while the remaining stages responded to the intermediate and highest doses not only of 17α-ethynylestradiol, but also 17β-estradiol, and nonylphenol. Moreover, fry have been shown to be the most sensitive of the salmon life stage on EDCs [23]. Czarny et al. [24] showed a dose-dependent effect of estrogens on the growth of cyanobacteria Microcystis aeruginosa. Concentrations below 1 mg/L did not affect the growth of cyanobacteria, whereas concentrations of hormones above 10 mg/L inhibited their growth. This is due to the phenomenon of hormesis. Low hormone concentrations activate the repair functions of cyanobacteria and induce the activity of proteins involved in them. Higher concentrations damage the maintenance and repair functions of cells. It was also observed that the effect of chronic toxicity depended on the hormone used and it decreased according to the series: 17-α-ethynylestradiol > progesterone > 17ß-estradiol > 5-pregnen-3β-ol-20-one > testosterone > estrone> levonorgestrel > estriol. Moreover, the hormone mixture caused a significant increase in toxicity compared to the same concentrations of individual hormones. The range of EC50 values obtained for the mixture of hormones and individual hormones were 56.66–166.83 mg/L and 88.92–355.15 mg/L, respectively (according to the EU classification, pollutants with EC50 values of 10–100 mg/L are harmful to aquatic organisms). The negative impact of hormones on cyanobacteria is connected with the rapid penetration of hormones into cells and the impact on photosynthetic activity by interfering with the flow of electrons through the photosystem II [24]. A significant increase in the toxicity of the mixture compared to individual substances may translate into more serious ecological effects. This observation is all the more important because of the environment where we usually deal with mixtures of hormones. Moreover, estrogens can accumulate in the food chain and the effects may appear in the next generation, threatening the health of the human population [4,11,24]. Also, the World Health Organization classified estrogens as group 1 carcinogens and some of their catechol metabolites such as 4-hydroxyestrone are also carcinogens [12,25]. Another group of endocrine substances that can be found in the environment are androgens. Like estrogens they can interfere with the normal functioning of the endocrine system of non-target organisms in trace concentration and they have many sources from which they get into the water, and due to filtration they also get into underground water. One of the most commonly identified androgens in the environment is testosterone, its presence in the environment may cause a high percentage of males in the aquatic environment, appearance of male secondary sex characteristics in female fish, inhibition of vitellogenin induction, reduction of reproductive capacity and masculinization in mammals [26]. For example, defeminisation has been observed in fathead minnows that have been exposed to wastewater from cattle farms [27]. Moreover, it has been showed that male Atlantic salmon exhibit an odorant response to testosterone at extremely low concentration (0.003 ng/L) [28]. There are also substances in the environment that disturb the action of endogenous compounds due to the similarity of their structure to hormones (chemicals mimic hormones), such as bisphenol A, 4-nonylphenol, parabens and phthalate, as well as antibacterial triclosan [29,30]. Moreover, some mycotoxins, such as zearalenone produced by several Fusarium spp., have strong estrogenic activity [31]. These compounds are resistant to microbiological degradation and their duration in sediments can be up to 40 years and, similar to hormonal substances, sometimes they can be food contaminants and thus, they can cause reproductive and developmental disorders of aquatic animals and humans [29,31]. Kriszt et al. [31] showed that zearalenone significantly increased the uterus weight in a dose dependent manner and upregulated complement component 2, calbindin-3 expression, Molecules 2020, 25, 4473 5 of 25 and decreased apelin and aquaporin 5 mRNA levels. This is due to the high affinity of zearalenone for estrogen receptors. Moreover, this compound and its metabolite α-zearalenol stimulate the proliferation of MCF-7 human adenocarcinoma cells [31]. Nonylphenol may cause various disorders of the male reproductive system, such as a reduction of testicle size and decrease of sperm production in Oncorhynchus mykiss. This mimic hormone was also observed to induce the proliferation of the human breast cancer cell line [32]. Due to the prevalence of endocrine compounds and other pharmaceuticals in the environment and their possible negative effect on non-target organisms, more and more attention is being paid to the methods of their removal from the environment. 3. Microbiological Degradation of EDCs In developed countries, where the problem of endocrine substances is the greatest, sewage treatment plants play a key role in their removal. Organisms involved in the removal of estrogens from the environment include bacteria, as well as fungi and microalgae (Figure 1) [11]. Figure 1. The main mechanisms for removing EDCs [3,9,26,30]. Bacteria that degrade these hormones belong to genera such as Bacillus, Virgibacillus, Novosphingobium, Rhodococcus, Acinetobacter, Pseudomonas, Sphingomonas, Enterobacter, Klebsiella, Aeromonas, Comamonas, Thauera, Deinococcus, Stenotrophomonas and cyanobacteria [ 28 31 33 39]. Raphidocelis subcapitata, Chlorella vulgaris, Chlorococcus and Scenedesmus quadricauda belong to algae capable of removing hormones [11 26 40 41]. Fungi from genus Trichoderma, 3,4,6,7,10,12,25, <ul style="display: flex;"><li style="flex:1">,</li><li style="flex:1">,</li><li style="flex:1">–</li></ul><ul style="display: flex;"><li style="flex:1">,</li><li style="flex:1">,</li><li style="flex:1">,</li></ul>Trametes, Phanerochaete, Pleurotus, Aspergillus, Lentinula, Drechslera, Curvularia, Penicillium, Acremonium, Fusarium, Gibberella, Beauvaria, Doaratomyces, Scopulariopsis, Chaetomidium, Thielavia, Neurospora, Absidia, Cunninghamella, Actinomucor, Rhizopus, Phycomyces, Mortierella, Circinella and Ganoderma (Table 2) were also described as being capable of hormone biodegradation/biotransformation [22,30,42–46]. Molecules 2020, 25, 4473 6 of 25 Table 2. Microorganisms engaged in EDCs biodegradation/biotransformation. <ul style="display: flex;"><li style="flex:1">Organism </li><li style="flex:1">EDCs </li><li style="flex:1">Dose </li><li style="flex:1">Efficiency [%] </li><li style="flex:1">References </li></ul>Virgibacillus halotolerans Bacillus flexus Bacillus licheniformis Novosphingobium sp. ARI-1 17β-estradiol 17β-estradiol 17β-estradiol estrone 5 mg/L 5 mg/L 5 mg/L 1.75 µg/L 1.52 µg/L 0.71 µg/L 30 mg/L 2 mg/L 100 100 100 80.43 100 94.76 94 [3] [3] [3] [4] [4] [4] [6] [7] [7] estriol 17β-estradiol 17β-estradiol 17α-ethynylestradiol 17α-ethynylestradiol Rhodococcus sp. JX-2 Rhodococcus zopfii Pseudomonas putida F1 Acinetobacter sp. 86.5 <ul style="display: flex;"><li style="flex:1">73.8 </li><li style="flex:1">0.5 mg/L </li></ul><ul style="display: flex;"><li style="flex:1">17β-estradiol </li><li style="flex:1">40 mg/L </li><li style="flex:1">90 </li><li style="flex:1">[10] </li></ul>DSSKY-A-001 Acinetobacter sp. LHJ1 Acinetobacter sp. BP8 Acinetobacter sp. BP10 Novosphingobium sp. SLCC Sphingomonas sp. KC8 17β-estradiol 17β-estradiol 17β-estradiol estrone 0.5 mg/L 1.8 mg/L 5 mg/L 100 100 100 no data 100 100 [10] [10] [10] [12] [25] [25] [25] [28] 1 mM <ul style="display: flex;"><li style="flex:1">estrone </li><li style="flex:1">0.05 mg/L </li></ul>0.05 mg/L 0.05 mg/L 1 mM 17β-estradiol testosterone testosterone 100 <ul style="display: flex;"><li style="flex:1">no data </li><li style="flex:1">Thauera sp. GDN1 </li></ul>

Suitability of Immobilized Systems for Microbiological Degradation of Endocrine Disrupting Compounds

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