Leng 2019

Chemosphere 238 (2020) 124680
Contents lists available at ScienceDirect
Chemosphere
journal homepage: www.elsevier.com/locate/chemosphere
Review
Use of microalgae based technology for the removal of antibiotics

from wastewater: A review
Lijian Leng a, Liang Wei a, Qin Xiong a, Siyu Xu a, Wenting Li a, Sen Lv a, Qian Lu a,
Liping Wan b, Zhiyou Wen a, c, **, Wenguang Zhou a, *
a
School of Resources, Environmental & Chemical Engineering and Key Laboratory of Poyang Lake Environment and Resource Utilization, Ministry of
Education, Nanchang University, Nanchang, 330031, China
b
Zhenghe Environmental Group, Nanchang, 330001, China
c
Department of Food Science and Human Nutrition, Iowa State University, Ames, IA, 50011, USA
h i g h l i g h t s g r a p h i c a l a b s t r a c t
Antibiotic toxicity and removal per-

formance depend on antibiotic and
algal species.
Antibiotic removal mechanisms are
mainly adsorption, accumulation,
and degradation.
Combining microalgae with irradia-
tion and oxidation favors antibiotic
degradation.
a r t i c l e i n f o a b s t r a c t
Article history: The antibiotic resistance induced by the release of antibiotics to the environment has urged research
Received 17 March 2019 towards developing effective technologies for antibiotic removal from wastewater. Traditional technol-
Received in revised form ogies such as activated sludge processes are not effective for antibiotic removal. Recently, microalgae-
29 July 2019
based technology has been explored as a potential alternative for the treatment of wastewater con-
Accepted 25 August 2019
Available online 26 August 2019
taining antibiotics by adsorption, accumulation, biodegradation, photodegradation, and hydrolysis. In
this review, the toxicities of antibiotics on microalgae, the mechanisms of antibiotic removal by
Handling Editor: Chang-Ping Yu microalgae, and the integration of microalgae with other technologies such as ultraviolet irradiation
(photocatalysis), advanced oxidation, and complementary microorganism degradation for antibiotic
Keywords: removal were discussed. The limitations of current microalgae-based technology and future research
Microalgal needs were also discussed.
Alga © 2019 Elsevier Ltd. All rights reserved.
Pharmaceutical and personal care products
(PPCPs)
Antibiotic resistance
Inhibitor toxicity
Wastewater treatment
* Corresponding author.
** Corresponding author. Department of Food Science and Human Nutrition, Iowa
State University, Ames, IA, 50011, USA
E-mail addresses: [email protected] (L. Leng), [email protected] (Z. Wen),
[email protected] (W. Zhou).
https://doi.org/10.1016/j.chemosphere.2019.124680
0045-6535/© 2019 Elsevier Ltd. All rights reserved.
2 L. Leng et al. / Chemosphere 238 (2020) 124680
Contents
1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2. Inhibition of antibiotics to microalgae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
3. Factors affecting antibiotic removal performance by microalgae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
3.1. Effect of algal species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
3.2. Effect of antibiotic classes and concentration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
3.3. Effects of algal growth conditions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
4. Antibiotic removal mechanisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
4.1. Adsorption . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
4.2. Accumulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
4.3. Biodegradation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
4.4. Photodegradation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
4.5. Hydrolysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9
5. Integration of microalgae-based antibiotic removal with other technologies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9
5.1. Ultraviolet (UV) irradiation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9
5.2. Advanced oxidation processes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9
5.3. Integration with other microorganisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10
6. Further research needs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10
6.1. The simultaneous removal of multiple antibiotics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10
6.2. The toxicity of degradation products . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
6.3. Accumulation of antibiotic resistance gene . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
7. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
1. Introduction Microalgae-based technology has also been introduced to treat

water or wastewater containing pharmaceutical and personal care
Antibiotics are commonly used to treat and prevent bacterial products (PPCPs). Studies have shown that microalgae can effec-
infections. Antibiotics such as penicillins, sulphonamides, cepha- tively remove PPCPs such as antibiotics from wastewaters (Bai and
losporins, macrolides, and quinolones have been widely used Acharya, 2016; Hom-Diaz et al., 2017; Villar-Navarro et al., 2018;
mainly in developing countries with 36% increase between 2000 Xiong et al., 2017a). For example, a high-rate algal pond (HRAP)
and 2010 (Thung et al., 2016). However, the prevalence of bacterial system dominated by Coelastrum sp. removed 64 PPCPs including
resistance is emerging as a significant concern due to the resultant 33 antibiotics (with an average concentration of 223 mg/L) from
higher medical costs, prolonged hospital stays, and increased municipal wastewater with average antibiotic removal rates being
mortality (Brown and Wright, 2016; Liu et al., 2016). 5e50% higher than the conventional activated sludge process
Wastewater treatment plants (WWTPs) are major sources of during a six-month-long process (Villar-Navarro et al., 2018). Wang
releasing antibiotics to the environment (Lai et al., 2017; Rizzo et al., et al. (2017) and Xiong et al. (2018b) summarized the potential of
2013). Due to the antibacterial natures, many antibiotics cannot be using microalgae to remove PPCPs. In the past three years, there has
effectively removed in WWTPs by activated sewage sludge, which is been a rapid increase in the number of publications related to
comprised of a group of bacteria (Baena-nogueras et al., 2017; Liu microalgae-based processes for antibiotics removal (Fig. 1). The aim
et al., 2018; Villar-Navarro et al., 2018). Many processes such as of the present review is to provide a comprehensive summary of
adsorption, advanced oxidation, and photocatalysis have been the recent progress of microalgae-based antibiotics removal pro-
studied to remove antibiotic (Homem and Santos, 2011; Tang et al., cess, with particular focus on the removal efficiency and mecha-
2016; Ternes et al., 2003; Wang et al., 2016; Wen et al., 2018; Zhou nisms. The current limitation in this area and future research
et al., 2017c). The antibiotic removal efficiency of adsorption process perspectives are also discussed.
is highly adsorbent-dependent, and the adsorbent is commonly
expensive (Ahmed et al., 2015; Tan et al., 2015). Advanced oxidation 2. Inhibition of antibiotics to microalgae
and photocatalysis may be generally effective but need intensive
expensive chemical agents or catalyst (Tang et al., 2016; Wen et al., The inhibition of microalgae induced by antibiotic is an impor-
2018; Jiang et al., 2018), in addition to the probable production of tant factor to consider in the development of algae-based antibiotic
secondary pollutants (Kang et al., 2012; Wang and Lin, 2012). On the removal processes. Antibiotics may affect algal growth through
other hand, microalgae wastewater treatment process is a biological inhibition of the synthesis of chemicals such as chlorophyll-a and
process and it needs few chemical agents and can be engineered to pigments and the activities of enzymes such as catalase and su-
effectively remove the emerging contaminants such as antibiotics peroxide dismutase (Perales-Vela et al., 2016; Bashir and Cho,
(Wang et al., 2017; Xiong et al., 2018b). 2016). Bashir and Cho (2016) reported that kanamycin and tetra-
Recently, microalgae-based technology has been widely re- cycline inhibited the growth and photosynthetic activity of Dic-
ported as an effective method to treat municipal and industrial tyosphaerium pulchellum and Micractinium pusillum through
effluents, with advantages such as CO2 fixation, contaminant regulating their protein synthesis. The decreased photosynthetic
removal, saving nutrients input, and potential of developing algae- activity of Chlorella vulgaris was observed when the alga was
derived products (Chen et al., 2015a; Bai and Acharya, 2019; Lu exposed to streptomycin (Perales-Vela et al., 2016). Species such as
et al., 2015; Zhou et al., 2011, 2012b, 2014, 2017a, 2017b). P. subcapitata, C. vulgaris, S. vacuolatus, and Desmodesmus
L. Leng et al. / Chemosphere 238 (2020) 124680 3
20 antibiotics. The same algal species (P. subcapitata) is even more

resistant to ampicillin and amoxicillin as 2000 mg/L of these two
antibiotics only resulted in 10% algal growth inhibition (Magdaleno
et al., 2015). Table 1 summarizes the concentrations of antibiotics
15 commonly present in WWTPs effluent and the EC50 values of those
antibiotics to specific algal species. Since the antibiotic concentra-
Number of publications
tions in WWTPs effluents are several orders of magnitudes lower

than the EC50 value, the use of the microalgae for treating antibi-
10 otics may be feasible after process development.
In general, the inhibitory effect of combined antibiotics can be
more severe than that caused by a single antibiotic. For example,
the 96 h-EC50 values of erythromycin, enrofloxacin, and
5
erythromycin-enrofloxacin mixture to C. vulgaris were 85.7, 124.5
and 39.9 mg/L, respectively, indicating the synergistic joint effect of
the two antibiotics (Wang et al., 2019). The inhibition of sulfa-
methoxazole and trimethoprim mixture on N. oculate was also
0
2009 2010 2011 2012 2013 2014 2015 2016 2017 2018
considerably higher than that of a single of the two antibiotics
(Teixeira and Granek, 2017). The adverse effects of tetracycline/
Publication year
oxytetracycline/chlortetracycline mixtures on the algal community
Fig. 1. Number of publications on the topic of “(microalga*) and (antibiotic) and were more significant than that of any single of these three anti-
(treatment or removal)” (data obtained from Web of Science on Jan. 10, 2019). biotics (Taşkan, 2016).
It should be noted that the use of growth-based EC50 value for
subspicatus are sensitive to antibiotics and thus are widely used as the assessment of antibiotic toxicity may not be universally appli-
biomarkers to monitor antibiotic contamination levels in the cable to evaluate the real toxicity of the substance. Other microalgae
environment (Va €litalo et al., 2017). activities such as photosynthesis, antioxidant system activities, and
The inhibitory effect of antibiotics on the microalgae is carotenoid biosynthesis can also be influenced by antibiotics and
commonly quantified through the half maximal effective concen- may be more indicative than biomass growth. For example, the
tration EC50, which is defined as the antibiotic concentration at photosynthesis activity of chlorophytes can be more sensitive than
which 50% of algal growth is inhibited. Most antibiotics have EC50 growth, as a result, the EC50 value based on the photosynthetic rate
values several orders of magnitudes higher than the concentrations of Desmodesmus subspicatus was only half of the EC50 based on cell
in wastewater or surface/groundwater, indicating microalgae number (growth-based) (Guo et al., 2016a). Therefore, additional
generally have good resistance to those antibiotics. For example, measures, along with cell growth, should be used in order to provide
the concentrations of ciprofloxacin, tetracycline, and sulfameth- a comprehensive insight into the impacts of antibiotics on algae and
oxazole are approximately 1 mg/L in municipal wastewater, while reveal the removal potential of the antibiotics.
the EC50 values of these antibiotics are 65 mg/L (to C. mexicana),
3.31 mg/L (to P. subcapitata), and 0.146 mg/L (to P. subcapitata), 3. Factors affecting antibiotic removal performance by
respectively (Va€litalo et al., 2017; Wang et al., 2017; Yang et al.,
microalgae
2005). In general, the EC50 value of an antibiotic depends on the
specific antibiotic and microalgae species, for example, sulfamo- 3.1. Effect of algal species
nomethoxine has an EC50 value of 5.9 to C. vulgaris and 9.7 mg/L to
Isochrysis galbana (Huang et al., 2014). For the alga P. subcapitata, The antibiotic removal rate highly depends on algal species.
the EC50 values of ciprofloxacin and gentamycin are 11.3 mg/L and Chlorella is very effective for the removal of many antibiotics. For
12.9 mg/L, respectively; while cephalotin and vancomycin show example, C. pyrenoidosa is commonly used to remove 7-amino
much higher EC50 values (>600 mg/L) (Magdaleno et al., 2015), cephalosporanic acid (7-ACA), amoxicillin, cefalexin, cefixime,
indicating the stronger resistance of P. subcapitata to these two cefradine, and ceftazidime (Table 2). Xiong et al. (2017a) studied the
Table 1
Concentrations of selected antibiotics in the environment and ecotoxicological effects.
Antibiotic Concentrations of antibiotics in effluent from municipal EC50 value (mg/L), time, species (ref.)
wastewater treatment plant (mg/L) (ref.)
Amoxicillin 1.34 (V€

alitalo et al., 2017) >50, 96 h, P. subcapitata (Va €litalo et al., 2017)
Cefradine 0.105 (Kim et al., 2017) 1.38, 72 h, M. aeruginosa (Chen and Guo, 2012)
1.77, 72 h, S. obliquus (Chen and Guo, 2012)
Cefalexin 0.13 (V€alitalo et al., 2017) 2.5 (Verlicchi et al., 2012)
Ceftazidime 3.68 (Liu et al., 2017b) >1.3 (Bengtsson-Palme and Larsson, 2016)
Ciprofloxacin 1.05 (Va€litalo et al., 2017) 65, 96 h, C. mexicana (Xiong et al., 2017c)
113, 72 h, P. subcapitata (Va€litalo et al., 2017)
Enrofloxacin 0.27 (V€
alitalo et al., 2017) 18.7, 72 h, P. subcapitata (Va€litalo et al., 2017)
5.57, 72 h, D. subcapicatus (Va €litalo et al., 2017)
Sulfamethazine <0.16 (Verlicchi et al., 2012) 1.231, 96 h, S. obliquus (Xiong et al., 2018c)
Sulfamethoxazole 1.94 (V€
alitalo et al., 2017) 0.146, 96 h, P. subcapitata (Va €litalo et al., 2017)
1.54, 24 h, S. vacuolatus (V€alitalo et al., 2017)
0.108, 96 h, S. obliquus (Xiong et al., 2018c)
Tetracycline 1.40 (V€
Tilmicosin 0.018 (Verlicchi et al., 2013) -a
Trimethoprim 1.15 (V€
a
Data not available.
4
Table 2
Removal of antibiotics by microalgae-based technology and removal mechanisms.
Antibiotic Microalgae-based technology Initial antibiotic concentration and removal rate, Wastewater category Removal mechanisms Ref.
hydraulic retention time
7-amino Chlorella sp. 100 mg/L and 100%, 97 h BM medium Adsorption > hydrolysis, photolysis Guo et al.
cephalosporanic acid Chlamydomonas sp. 100 mg/L and 100%, 135 h BBM medium (2016b)
(7-ACA) Mychonastes sp. 100 mg/L and 100%, 135 h BG-11 medium
7-ACA C. pyrenoidosa 40 mg/L and 96.1%, 24 h (light) BG-11 medium Adsorption, biodegradation Yu et al. (2017)
Amoxicillin C. pyrenoidosa 100e300 mg/L and 100%, over 48 h BG-11 medium Algal action Li et al. (2015)
400e500 mg/L and 83e89%, 36e48 h
C. pyrenoidosa þ H2O2/Fe2þ 1 g/L and 93.3%, 48 h Algal action > Fenton oxidation
Amoxicillin S. obliquus þ UV irradiation 100 mg/L and 98.5%, 24 h (UV irradiation at 280 nm BG-11 media Photodegradation, biodegradation, and Yang et al. (2017)
for 5 min) hydrolysis
Selenastrum capricornutum þ UV irradiation 100 mg/L and 85.8%, 24 h (UV irradiation at 365 nm
for 5 min)
C. pyrenoidosa þ UV irradiation 100 mg/L and 85%, 24 h (UV irradiation at 365 nm
for 5 min)
Antibiotic mixtures a
Mixture of algae-bacteria consortia (dominanted 28e1054 mg/L, 38.6e97.8%, 144 h Real domestic wastewater -b Villar-Navarro
by Coelastrum sp.) in HRAP et al. (2018)
Cefradine C. pyrenoidosa 100e500 mg/L and 7e23%, 48 h BG-11 medium Algal action Li et al. (2015)
C. pyrenoidosa þ H2O2/Fe2þ 1 g/L and 92.2%, 48 h Algal action > Fenton oxidation
Cefalexin C. pyrenoidosa 10 mg/L and 94.9%,48 h BG-11 medium Algal action > self-degradation Guo and Chen
L. Leng et al. / Chemosphere 238 (2020) 124680

(2015)
Cefalexin Nonliving lipid-extracted Chlorella sp. 49.17 mg/L and 71.2%, 2 h Deionized water Adsorption Angulo et al.
Nonliving Chlorella sp. 49.17 mg/L and 82.8%, 7 h Deionized water Adsorption (2018)
Cefalexin C. vulgaris þ UV irradiation 40 mg/L and 97.15%, 24 h (UV irradiation at 280 nm EPA medium Photodegradation Liu et al. (2017b)
for 1 h)
C. pyrenoidosa þ UV irradiation 1.1 mg/L and 99.23% 24 h (UV irradiation at 185 nm Photodegradation Liu et al. (2017b)
for 1 h)
Cefixime C. pyrenoidosa 10 mg/L and 100%,48 h BG-11 medium Algal action > self-degradation Guo and Chen
(2015)
Cefradine C. pyrenoidosa 10 mg/L and 89.9%,48 h BG-11 medium Algal action > self-degradation Guo and Chen
(2015)
C. pyrenoidosa þ activated sludge 100 mg/L and 97.9%,48 h Algal action > activated sludge Guo and Chen
(2015)
Cefradine C. pyrenoidosa 30 mg/L and 75.9%, 48 h BG-11 medium Algal degradation Chen et al.
60 mg/L and 54.6%, 48 h (2015b)
Cefradine S. obliquus þ UV irradiation 100 mg/L and 62.5%, 24 h (UV irradiation at 365 nm BG-11 media Photodegradation, biodegradation, and Yang et al. (2017)
for 5 min) hydrolysis
Selenastrum capricornutum þ UV irradiation 100 mg/L and 61.8%, 24 h (UV irradiation at 365 nm
for 5 min)
C. pyrenoidosa þ UV irradiation 100 mg/L and 29.4%, 24 h (UV irradiation at 365 nm
for 5 min)
Ceftazidime C. pyrenoidosa 10 mg/L and 89.7%,48 h BG-11 medium Algal action > self-degradation Guo and Chen
(2015)
Ceftazidime C. pyrenoidosa 40 mg/L and 92.7%, 6 h (light) BG-11 medium Adsorption, biodegradation Yu et al. (2017)
Ceftazidime C. pyrenoidosa 40 mg/L and 80e99.2% in 6 h (depending on BG-11 media Biodegradation, photodegradation, Du et al. (2015b)
different light and nutrient supply) adsorption and hydrolysis
Ciprofloxacin Chlamydomonas mexicana 2 mg/L and 13.0%, 11 d Bold's Basal Medium Biodegradation, accumulation and Xiong et al.
adsorption (2017c)
C. pitschmannii 2 mg/L and 1.6%, 11 d
O. multisporus 2 mg/L and 2.0%, 11 d
C. vulgaris 2 mg/L and 0, 11 d
Chlamydomonas mexicana 2 mg/L and 56%, 11 d Bold's Basal Biodegradation > accumulation, adsorption
Medium þ sodium acetate
(4 g/L)
Ciprofloxacin Nannochloris sp. 57 ng/L and 100%, 7 d Water from Las Vegas Wash Direct photolysis Bai and Acharya
(2017)
Ciprofloxacin Mixture of algae-bacteria consortia in pilot high 1.31 mg/L and 20.1%, 24 h (8 h sunlight/16 h dark) Real domestic wastewater Photodegradation during daytime, and Hom-Diaz et al.
rate algae pond (HRAP) adsorption during night time (2017)
Mixture of algae-bacteria consortia in 1-L HRAP 1.11 mg/L and 83.8%, 24 h Photodegradation
Enrofloxacin S. obliquus 1 mg/L and 23%, 11 d Bold's Basal Medium Biodegradation > accumulation, adsorption Xiong et al.
(2017a)
Chlamydomonas mexicana 1 mg/L and 25%, 11 d
C. vulgaris 1 mg/L and 26%, 11 d
Ourococcus multisporus 1 mg/L and 18%, 11 d
Micractinium resseri 1 mg/L and 20%, 11 d
Microalgae consortia of the above five species 1 mg/L and 26%, 11 d
Florfenicol Chlorella sp. 46 mg/L and 97% BG-11 medium Biodegradation > accumulation, adsorption Song et al. (2019)
159 mg/L and 74%
Levofloxacin C. vulgaris 1 mg/L and 91.5%, 11 d Bold's Basal Medium þ1% Accumulation and biodegradation Xiong et al.
L. Leng et al. / Chemosphere 238 (2020) 124680

NaCl w/v (2017b)
Sulfamethazine Scenedesmus obliquus 0.025e0.25 mg/L and 31.4e62.3%, 12 d Bold's Basal Medium e Xiong et al.
(2019)
Sulfamethoxazole Scenedesmus obliquus 0.025e0.25 mg/L and 27.7e46.8%, 12 d Bold's Basal Medium e Xiong et al.
(2019)
Sulfamethoxazole Nannochloris sp. 10 mg/L and 32%, 14 d (12 h light/12 h dark) F/2 medium Algae-mediated photolysis Bai and Acharya
(2016)
Sulfamethoxazole Nannochloris sp. 360 ng/L and 11%, 14 d Water from Las Vegas Wash Algae-mediated photolysis, accumulation Bai and Acharya
(2017)
Sulfamethoxazole C. pyrenoidosa 2e8 mg/L and 48.5e69.9%, 13 d F/2 medium Accumulation and biodegradation Sun et al. (2017)
Tetracycline Algae with activated sludge 2 mg/L and 97%, 24 h (12 h light and 12 h dark) Real domestic wastewater Photodegradation, biodegradation, Norvill et al.
adsorption and hydrolysis (2017)
Tilmicosin Chlorella PY-ZU1 0.01e50 mg/L and 90.2e99.8%, 9 d SE medium Adsorption, photodegradation, and Cheng et al.
biodegradation (2017)
Trimethoprim Nannochloris sp. 1.6 ng/L and 11%, 350 h Water from Las Vegas Wash Biodegradation, photolysis Bai and Acharya
(2017)
Trimethoprim Nannochloris sp. 10 mg/L and 0, 14 d F/2 medium e Bai and Acharya
(2016)
a
The concentrations (mg/L) and removal rates (%) for some major antibiotics are: ofloxacin, 704 and 83.9; ciprofloxacin, 918 and 73.4; norfloxacin, 513 and 88.7; azithromycin, 290 and 55.9; erythromycin, 173 and 91.3;
clarithromycin, 1054 and 97.8; spiramycin, 321 and 96.9; tetracycline, 296 and 43.6; chloramphenicol, 46 and 91.3; sulfadiazine, 44 and 38.6; trimethoprim, 252 and 40.5; metronidazole, 28 and 39.3.
b
No removal or not reported.
5
removal of levofloxacin by various species including C. vulgaris, as Chlamydomonas mexicana, C. pitschmannii, O. multisporus, or
Chlamydomonas mexicana, Chlamydomonas pitschmannii, Our- C. vulgaris (Xiong et al., 2017c) even the concentration was at a
ococcus multisporus, Micractinium resseri, and Tribonema aequale relatively low level (2 mg/L). Similarly, only 18e25% of enrofloxacin
and reported that C. vulgaris achieved a higher removal rate than (1 mg/L) was removed by S. obliquus, Chlamydomonas mexicana,
other species. In another study, the same group also reported that C. vulgaris, Ourococcus multisporus, or Micractinium resseri (Xiong
C. vulgaris was more effective to remove enrofloxacin than et al., 2017b). Clearly, ciprofloxacin and enrofloxacin are more
S. obliquus, Chlamydomonas mexicana, Ourococcus multisporus, and difficult to be removed than 7-ACA. It is interesting that the pres-
Micractinium resseri (Xiong et al., 2017b). The antibiotic removal by ence of multiple antibiotic classes may enhance their removal ef-
other algal species may be less effective. For example, the removal ficiency by using microalgae. For example, when S. obliquus was
rates of spiramycin and amoxicillin by Microcystis aeruginosa were used to remove the antibiotic sulfamethazine, the removal rate
12.5e32.9% and 30.5e33.6%, respectively (Liu et al., 2012). The increased from 18.5-23.6% to 38.2e51.8% when another antibiotic
removal of ciprofloxacin by Chlamydomonas mexicana was also sulfamethoxazole was added to the system (Xiong et al., 2018a).
limited to 13% (Xiong et al., 2017c). Nannochloris sp. had limited Sulfamethoxazole may have increased the activities of cytochromes
removal rate for trimethoprim (0e11%) and sulfamethoxazole P450 enzyme, such as aminopyrine N-demethylase and aniline
(11e32%) (Bai and Acharya, 2017, 2016). However, studies have also hydroxylase (Xiong et al., 2018a), which may have higher affinity
found some antibiotics more vulnerable to other algal species than toward sulfamethazine than sulfamethoxazole.
to Chlorella. For example, cefradine can be removed by more than
60% using S. obliquus, while the removal by C. pyrenoidosa was less 3.3. Effects of algal growth conditions
than 30% (Yang et al., 2017).
Development of robust algal strains for antibiotic removal can The growth conditions of microalgae including nutrients, pH,
be accomplished through various approaches. A large pool of algae illumination, temperature, CO2 concentration, salinity, design of
species in the nature provides the possibility to isolate robust the photobioreactor, dissolved oxygen, and algal growth inhibitors
strains that can tolerate antibiotics (Leng et al., 2018; Zhou et al., are critical to the antibiotic removal efficiency (Norvill et al., 2016).
2017a). The polyculture of multiple algal strains with comple- In general, favorable algal growth conditions are beneficial to the
mentary antibiotic removal capabilities may also increase the effi- removal of antibiotics.
ciency and stability of the microalgae-based antibiotic removal Addition of appropriate nutrients can promote the algal growth
system (Godwin et al., 2017). In addition, genetic modification and metabolisms, leading to enhanced antibiotic removal performance.
metabolic evolution of the algal strain can also enhance antibiotic For example, addition of 4 g/L sodium acetate to Chlamydomonas
removal efficiency (Shen et al., 2015). It was reported that genetic Mexicana cultures enhanced ciprofloxacin removal by more than 3
adaptation and physiological acclimatization contributed to the times (Xiong et al., 2017c) and addition of NaCl (1%, wt) to
increased tolerance of N. oceanica to Zeocin (Lin et al., 2017) and the C. vulgaris culture resulted in 3-fold higher levofloxacin removal
enhanced levofloxacin removal by C. vulgaris (Xiong et al., 2017a). than the control (Xiong et al., 2017a). The same group also reported
that the removal of levofloxacin by S. obliquus can be increased
3.2. Effect of antibiotic classes and concentration from 4.5% to 93.4% with the increase of salinity from 0 to 171 mM
NaCl (Xiong et al., 2017d). NaCl (salinity stress) promoted the bio-
Microalgae-based antibiotic removal also highly depends on the accumulation and subsequent intracellular biodegradation of lev-
antibiotic concentrations and classes. Most antibiotics pose in- ofloxacin, due possibly to the increased quantity of ferroxidase-like
hibitions on algal growth when the concentration is close to or protein, which can direct electrons toward cytochrome P450-
higher than the algal tolerable level. As the antibiotic concentra- catalyzed hydroxylation of levofloxacin (Xiong et al., 2017d).
tions commonly studied are in the magnitude of several mg/L to The pH of the algal growth system can mediate the hydrolysis of
hundreds of mg/L (Table 2), which are comparable to or even higher some ionic antibiotics, and thus pH is crucial to the removal effi-
than the corresponding EC50 values (Table 1), low antibiotic ciency for those antibiotics. An alkaline pH can change the ionic
removal rates would be expected (Chen et al., 2015b; Li et al., 2015; state of tetracycline due to the hydrolysis of this antibiotic,
Sun et al., 2017). However, it should be noted that the increasing enhancing its removal efficiency (Norvill et al., 2017). Trimethoprim
antibiotic concentration within a certain range may have little in- and sulfamethoxazole were in a stable form when pH was slightly
fluence on its removal when the concentration is within algal basic and thus underwent slow direct photolysis (Bai and Acharya,
tolerable level. For example, the critical toxic concentration for 2017). However, Guo et al. (2016b) reported that the pH variation
amoxicillin to C. pyrenoidosa was 300e400 mg/L (Li et al., 2015). did not affect 7-ACA removal rate, due to the reason that 7-ACA is
Different antibiotic has diverse critical concentration, and that of relatively stable at the pH range (6.3e8.0) studied.
tilmicosin to Chlorella PY-ZU1 was ~30 mg/L (Cheng et al., 2017). Illumination causes photodegradation of antibiotics, and thus it
Interestingly, greater removal rates of sulfamethazine and sulfa- can be used to improve antibiotic removal efficiency (Du et al.,
methoxazole in higher concentration mixtures were observed than 2015a). Strong light irradiation can also increase dissolved oxygen
those in lower ones possibly because of the efficient adaptive and pH due to the elevated photosynthesis of microalgae, which in
mechanism of Scenedesmus obliquus to these antibiotics (Xiong turn induced the generation of reactive oxygen species and
et al., 2019). enhanced tetracycline removal (Norvill et al., 2017).
The removal efficiency of antibiotics by microalgae also highly Other algal growth conditions also play important roles in
depends on antibiotic classes. Different antibiotic kinds, even at a antibiotic removal. It is reported that during a six-month operation
similar concentration level, can result in significantly different in HRAP, increasing temperature by 10 C and irradiance by 20 MJ/
removal efficiencies. For example, microalgae C. pyrenoidosa can m2/d considerably promoted the removal of antibiotics such as
remove 83e100% amoxicillin, but can only remove 7e23% cefradine ofloxacin, ciprofloxacin, and norfloxacin (Villar-Navarro et al.,
(Li et al., 2015) even the two antibiotics were at the same concen- 2018). The inoculum size and the hydraulic retention time of the
tration. When 7-ACA (40e100 mg/L) was treated by Chlorella sp., microalgae growth system should also be adjusted based on the
Chlamydomonas sp., Mychonastes sp., or C. pyrenoidosa, 96e100% antibiotic concentration and algal species (Bengtsson-Palme and
removal rate can be achieved (Guo et al., 2016b; Yu et al., 2017). Larsson, 2016; Heidari et al., 2016). In addition, algae can use an
However, only 0e13% of ciprofloxacin was removed by strains such extended lag phase to adapt the algae to an extremely hostile
environment such as the sharp increase of the tetracycline con- tetracycline in HRAP (Godos et al., 2012; Norvill et al., 2017). The
centration from 1 mg/L to 20 mg/L (Xiong et al., 2018d) and the adsorption process is generally fast, e.g., 7-ACA can be removed by
presence of inhibitory compounds such as N-heterocyclic com- microalgae adsorption within 10 min (Guo et al., 2016b). The
pounds (Godwin et al., 2017; Tommaso et al., 2015). adsorption of antibiotic by microalgae biomass is mainly achieved
through hydrogen bonds, electrostatic attraction, partition, and
4. Antibiotic removal mechanisms hydrophobic effect (Ahmed et al., 2015; Tan et al., 2015) (Fig. 3). In
some other studies, adsorption was not a dominant antibiotic
When exposed to antibiotics, microalgae display a series of re- removal mechanism, but it can act as the first process for the af-
sponses to survive and remove the toxic antibiotics. During the terward microalgae-based antibiotic removal mechanisms such as
removal process, adsorption, accumulation, biodegradation, pho- accumulation and biodegradation (Yu et al., 2017).
todegradation, and hydrolysis of antibiotics may take place (Table 2
and Fig. 2).
4.1. Adsorption 4.2. Accumulation
Adsorption is the process of removing pollutants by passive Unlike adsorption which is extracellular, accumulation is an
binding of the pollutants to a solid material (Bai and Acharya, 2016; intracellular process to remove pollutant from water (Bai and
Davis et al., 2003). The removal of antibiotics by adsorbent such as Acharya, 2016; Davis et al., 2003). Some antibiotics can cross algal
biochar, activated carbon, and nano-materials has been extensively cell membranes and then possibly be assimilated by the cells. The
reported (Ahmed et al., 2015; Huang et al., 2017; Xiong et al., 2018c; intracellular accumulated antibiotics may be extracted by sonicat-
Zhang et al., 2016; Zhou et al., 2017d). Microalgae can be an effec- ion coupled with dichloromethane/methanol mixture (v:v ¼ 1:2)
tive adsorbent for antibiotics removal. The adsorption can be extraction (Song et al., 2019). Algae accumulation has been re-
accomplished by the functional groups and polymer assemblages ported played an important role in the removal of antibiotics such
(similar to cellulose, hemicelluloses, and proteins, etc.) on the algal as trimethoprim, sulfamethoxazole, and doxycycline (Bai and
cell walls and it is an extracellular process (Davis et al., 2003; Xiong Acharya, 2017; Prata et al., 2018).
et al., 2018b). The effectiveness of the adsorption process may be Some accumulated antibiotics can induce the production of
assessed by using dead algal biomass to adsorb antibiotics, and reactive oxygen species which is essential to control cellular
adsorption performance varies significantly depending on specific metabolism at normal concentrations, but resulting in severe
antibiotics and microalgae due to their different hydrophilicity, damage to cells or eventually death if in excess (Xiong et al., 2018a).
functionality, and structures. In general, it is desirable when the On the other hand, the algal cell can counteract to deplete the
antibiotic is more hydrophobic rather than hydrophilic and when it antibiotics by metabolism. In this case, accumulation becomes a
carries an opposite charge to microalgae (Leng et al., 2015; Xiong pre-step for biodegradation (described in Section 4.3), and the
et al., 2018b). combination of accumulation and biodegradation in algal cells
Some antibiotics can be removed effectively by adsorption. For contribute considerably to the completion of the assimilation of
example, 82.7% and 71.2% of the cefalexin (at 50 mg/L) in modeling some antibiotics. The accumulation of sulfamethazine in
wastewater can be removed by Chlorella sp. biomass and the de- C. pyrenoidosa was observed and then followed by biodegradation
fatted biomass of Chlorella sp., and the calculated theoretical (Sun et al., 2017). Levofloxacin was also removed by C. vulgaris
adsorption capacities were 129 and 63 mg/g, respectively (Angulo through accumulation and subsequent intracellular biodegradation
et al., 2018). Very high adsorption capacity (295 mg/g) was ob- (Xiong et al., 2017a). Otherwise, antibiotics will be accumulated in
tained when using lipid-extracted S. quadricauda biomass to the organisms, and the antibiotics can further accumulate and
remove tetracycline (Daneshvar et al., 2018). Adsorption was also magnify through the food chain and eventually cause antibiotic
found to be one of the main mechanisms for the removal of resistance in the human body.
Fig. 2. Antibiotic degradation and detoxification mechanisms by microalgae.

Fig. 3. Possible mechanisms during the adsorption of antibiotics, adapted from (Tan et al., 2015) with permission.
4.3. Biodegradation can be treated as a two-phase enzymatic catalysis process. In the

first phase, antibiotics can be enzymatically hydrolyzed, oxidized,
Biodegradation describes the process of breaking down antibi- or reduced to more hydrophilic compounds using enzymes such as
otics by algae within or outside the cells, with some broken-down monooxygenase and dioxygenase (Xiong et al., 2016), while in the
derivatives being further consumed by the algal cells (Gao and Chi, second, the hydrophilic compounds can be catalyzed by another
2015; Ke et al., 2010; Naghdi et al., 2018; Zhou et al., 2013a). An group of enzymes such as glutathione-S-transferases to produce
example of this mechanism is the intracellular degradation of cef- smaller molecules with lower toxicity (Xiong et al., 2018b), e.g.,
tazidime and its basic parent structure 7-ACA by C. pyrenoidosa. In resulting in the opening of the epoxide ring of antibiotics to protect
this process, the removal of antibiotics was proceeded in three against oxidative damage to algal cell (Ding et al., 2017).
steps: ceftazidime was firstly adsorbed on algae, then it was slowly Irrespective of the different antibiotic removal mechanisms
transmitted algal cell wall, and finally, it was broken down by algal discussed above, hydrolysis, side chain breakdown, hydroxylation,
enzymes (Yu et al., 2017). Other intracellular degradation-based ring cleavage, demethylation, decarboxylation, and dehydrox-
antibiotics removal cases include levofloxacin removal by ylation of antibiotics may take place when biodegrading antibiotics
S. obliquus (Xiong et al., 2017d) and its removal by C. vulgaris (Xiong (Chen and Xie, 2018; Xiong et al., 2017d, 2018a), e.g., biodegrada-
et al., 2017a). For the extracellular degradation process, the anti- tion mechanisms of levofloxacin as shown in Fig. 4 include several
biotic is broken down by algal metabolites such as extracellular of these reactions.
enzymes, and the biodegraded intermediates/end-products may be
further metabolized by algal cells (Naghdi et al., 2018). The con- 4.4. Photodegradation
tributions of the intracellular and extracellular mechanisms for
antibiotic removal may be differentiated by analyzing the antibiotic Photodegradation of antibiotics includes direct photolysis of
intermediates/end-products in the medium and in biomass or by antibiotics contributed by light and their indirect photodegradation
using extra- and intra-cellular enzymes extracted from algae to which is induced by the reactive components produced by algae in
degrade antibiotics. the presence of light.
Algal metabolism for antibiotic degradation can be classified as, Many antibiotics can be removed by direct photolysis in the
co-metabolic degradation and metabolic degradation patterns. Co- presence of light in algae-free conditions (Chen et al., 2016; Jiang
metabolic degradation uses non-specific enzymes to degrade the et al., 2018). By comparing the removal rate between daytime and
antibiotics with additional carbon and energy input is needed, night, it was found that 40% of tetracycline in water can be removed
while in the metabolic degradation process, algae utilize antibiotics by direct sunlight (Norvill et al., 2017). The removal of tetracycline
as the sole carbon and energy sources with specific enzymes. Both (Godos et al., 2012), ciprofloxacin (Bai and Acharya, 2017), cefazolin
of these two patterns contributed to levofloxacin biodegradation by and cephapirin (Wang and Lin, 2012) in different microalgae-based
C. vulgaris (Wang et al., 2017; Xiong et al., 2017a). Augmentation by wastewater treatment systems were also reported to be a result
the addition of organic substrates such as methanol or sodium from direct photolysis.
acetate can promote the biodegradation of ciprofloxacin because of The removal of certain antibiotics can be enhanced through
co-metabolism (Xiong et al., 2017c). indirect photodegradation when algae present in the system. Dur-
Based on enzyme functionalities, the antibiotic biodegradation ing indirect photodegradation, reactive oxygen species such as
4.5. Hydrolysis
The break-down of some antibiotics can also be accomplished

by hydrolysis. It should be noted that hydrolysis reactions induced
by algal metabolites such as enzymes (enzymatic hydrolysis) can
also be regarded as biodegradation processes. Hydrolysis of 7-ACA
contributed to the removal of the b-lactam antibiotic due to the
ring-opening reactions of the b-lactam structure (Guo et al., 2016b).
Hydrolysis pathways for b-lactam antibiotic ampicillin varied
significantly depending on aqueous pH and temperature (Fig. 6);
increasing pH and temperature considerably increased the hydro-
lysis rates (Mitchell et al., 2014). Note that growth of algae may
change the pH of the culture, e. g, pH increase because of the
photosynthetic activity of microalgae, hydrolysis of pH-sensitive
antibiotics can be greatly influenced by these algae.
Hydrolysis reactions increased the polarity and hydrophilicity of
antibiotics and therefore facilitated antibiotics solubilization and
subsequent biodegradation by microalgae (Wang et al., 2018). Some
antibiotics such as fluoroquinolones and sulphonamides were
resistant to hydrolysis, e.g., sulphadiazine and sulphaguanidine
ska et al.,
were hydrolytically stable at pH as low as 4.0 (Białk-Bielin
2012). Hydrolysis of tetracycline barely contributed to its removal
by microalgae (Norvill et al., 2017).
5. Integration of microalgae-based antibiotic removal with

other technologies
Fig. 4. Possible metabolic pathways of levofloxacin, reprinted from (Xiong et al.,
2017d) with permission.
5.1. Ultraviolet (UV) irradiation
hydroxyl radical can be generated from algal components, leading UV irradiation is a commonly used disinfection step in the
to the break-down of the antibiotics. For example, when light wastewater treatment and can enhance antibiotic removal by direct
presented in the C. vulgaris culture, hydroxyl radical was generated, and indirect photodegradation. Light-sensitive antibiotics can be
resulting in rapid oxidation of norfloxacin (Zhang et al., 2012a). In removed by UV irradiation through direct photolysis. During UV
algae-bacteria based HRAP, tetracycline was removed almost irradiation, antibiotics absorb photons which can break some
completely due to the indirect photodegradation mediated by dead chemical bonds of antibiotics (Du et al., 2015b; Liu et al., 2017b).
or active algal cells (Norvill et al., 2017). Indirect photodegradation The resulted products were vulnerable to microalgae biodegrada-
also contributed to the removal of ciprofloxacin (Hom-Diaz et al., tion (Liu et al., 2017b). Yuan et al. (2011) reported a rapid degra-
2017), cefalexin and cephradine (Wang and Lin, 2012). Both direct dation of doxycycline in the presence of UV light. More than 73% of
and indirect photodegradation contributed to cephradine removal the cefradine (initial concentration of 150 mg/L) was removed with
and the photodegradation products and degradation pathways of UV irradiation (Du et al., 2015b).
cephradine are shown in Fig. 5. UV irradiation can be combined with microalgae treatment to
However, some antibiotics are recalcitrant to light and the light- enhance antibiotic degradation through indirect photodegradation.
induced algal reactive species. In these circumstances, photo- Since UV light attenuates rapidly in wastewater within the range of
degradation is not effective for antibiotic removal. For example, several centimeters to decimeters (Curtis et al., 1994), indirect
sulfamethoxazole was only removed slightly (11%) in the presence photodegradation can be the dominant mechanism for antibiotic
of Nannochloris sp. and light after 14-day cultivation (Bai and removal. Although individual algae C. pyrenoidosa was inefficient to
Acharya, 2017). No photodegradation was observed when levo- remove cefradine (<20%), the integrated algae-UV irradiation ach-
floxacin was treated with S. obliquus (Xiong et al., 2017d). ieved a high cefradine removal rate (>78%) and reduced the toxicity
of the effluent by more than 50% (Du et al., 2015b). UV irradiation
was also a trigger for S. obliquus treatment of cefradine and amox-
icillin, a complete removal of these antibiotics were obtained when
coupling S. obliquus with UV irradiation (Yang et al., 2017). However,
it should be noted that UV irradiation (280e320 nm) may pose a
negative effect on algal growth and biochemical compositions
(Kumar et al., 2018). The use of UV-mutated algal species may be
favorable to avoid the negative effect of UV on algae (Liu et al., 2015).
5.2. Advanced oxidation processes
Advanced oxidation processes (AOPs) have been developed as a

pretreatment step to enhance the efficiency of the treatment of
wastewater containing recalcitrant organic compounds such as
Fig. 5. Possible direct and indirect photodegradation products and degradation path- antibiotics (Cheng et al., 2018; Guan et al., 2018; Liu et al., 2017a).
ways of cephradine, reprinted from (Wang and Lin, 2012) with permission. During the AOPs-algae treatment, the antibiotics can be removed
Fig. 6. Possible hydrolysis pathways for ampicillin in water at pH 4, 7, and 9 and 60 C: (a) amide hydrolysis and decarboxylation; (b) lactam hydration with acetic acid; (c)
ampicillin isomer; (d) lactam hydration; (e) lactam hydration isomer; (f) lactam hydration and decarboxylation, reprinted from (Mitchell et al., 2014) with permission.
directly by oxidation reactions. For example, the removal of competitive interactions such as the adverse effects on each other,
amoxicillin and cefradine by microalgae increased from 7.4 to 22.5% e.g., the excretion of algicidal or bactericidal substances (Gonçalves
to over 90% when coupling H2O2/Fe(II)-based Fenton reactions (Li et al., 2017). A C. pyrenoidosa-activated sludge integration system
et al., 2015). Fenton reactions enhanced the biodegradability of was applied to effectively remove cefradine, and a removal effi-
intermediates produced by the advanced oxidation of the antibi- ciency of 97.9% was obtained (Guo and Chen, 2015). Pretreatment of
otics (Li et al., 2015). wastewater containing amoxicillin as high as 150 mg/L by Chlorella
On the other hand, antibiotics can also be removed by AOPs- sp.-bacteria consortium in intertidal wetland sediment or activated
induced indirect photodegradation. For example, the presence of sludge resulted in >99% removal of the antibiotic (Shi et al., 2018).
photochemically reactive Fe(III) can induce reactive oxygen species The antibiotic biodegradation products from algae may be more
formation which in turn promoted the antibiotic removal by biodegradable to bacteria and vice versa. The complementary
microalgae (Batista et al., 2014). The addition of Fe(III) can also degradation characteristics of multiple microorganisms and the
enhance the photodegradation of norfloxacin by microalgae (Zhang possible exchange of antibiotic degradation products between
et al., 2012a). Ge and Deng (2015) reported the use of Fe(III)- algae and bacteria may have promoted the effectiveness of antibi-
microalgae system to effectively remove the two fluoroquinolone otics removal (Guo and Chen, 2015; Mun ~ oz and Guieysse, 2006).
antibiotics, enrofloxacin and ciprofloxacin hydrochloride. However, However, the photo-bioreactors for the microalgae-bacteria mixed
when using Fenton reagents in the algae-based antibiotic removal, culture were not effective for tetracycline removal at high con-
the dosage of Fenton reagents should be adjusted delicately as high centrations (Xiong et al., 2018d). In addition to bacteria, fungus is
concentrations of H2O2 or Fe(II) can be lethal to microalgae (Li et al., another candidate to assist antibiotic removal with algae (Naghdi
2015). et al., 2018). For example, the removal of antibiotic ranitidine by
C. vulgaris-Aspergillus niger biopellets was reported effective (Bodin
5.3. Integration with other microorganisms et al., 2016).
Co-culture of multiple microalgae species and the co-culture of
The performance on antibiotic removal by microalgae can be microalgae with bacteria or fungi may be more cost-effective for
enhanced by coupling with other microorganisms such as bacteria antibiotic wastewater treatment. Note that the microalgae may be
and fungi. Many bacterial strains are capable of removing antibi- easily harvested after co-culturing with bacteria or fungi (Chen
otics (Wang et al., 2017). For example, sulfapyridine and sulfathia- et al., 2018; Zhou et al., 2012a, 2013b), the integrated use of
zole can be biodegraded effectively by bacteria Escherichia sp. HS21 microalgae with other microorganisms worth further in-
or Acinetobacter sp. HS51 (Zhang et al., 2012b). Sulfamethoxazole vestigations. On the other hand, whether if the co-culture can
was removed effectively by Pseudomonas psychrophila HA-4 due to contribute to the antibiotics resistance genes reducing is also a
the efficient complementary algal metabolic biodegradation (Jiang research front of this technology.
et al., 2014). The fast biodegradation of ciprofloxacin by Thermus sp.
isolated from pharmaceutical sludge was also reported (Pan et al., 6. Further research needs
2018).
The use of algal-bacterial consortia for removal of hazardous 6.1. The simultaneous removal of multiple antibiotics
contaminants has attracted increasing interests (Mun ~ oz and
Guieysse, 2006). Within the algal-bacterial symbiotic relationship, Many studies have focused on the removal of a single antibiotic
Oxygen needed for bacteria can be photosynthetically produced by class. The removal of the multiple antibiotics by microalgae is only
microalgae in the presence of light and CO2, which is produced by occasionally studied. In real wastewater, however, multiple anti-
bacteria when oxidizing organic matter (Quijano et al., 2017). Other biotics and other contaminants will most likely to co-exist. In
interactions between these microorganisms include cooperative general, antibiotic removal efficiency is algal strain dependent and
interactions such as the use of microalgae as a protecting habitat for antibiotic class-specific (Li et al., 2015; Ribeiro et al., 2018). In-
bacteria to enhance bacterial growth, in addition to possible teractions between different antibiotics or between antibiotics and
other substances make the microalgae removal process more Acknowledgments

complicated. Future investigations are needed to assess the
possible adverse effects of multi-antibiotic. The study was supported by the major research and develop-
ment program of Jiangxi, China (No. 20182ABC28006) and the
6.2. The toxicity of degradation products National Natural Science Foundation of China (Nos. 51808278 and
51668044).
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Chemosphere 238 (2020) 124680

Contents lists available at ScienceDirect

Use of microalgae based technology for the removal of antibiotics

Antibiotic toxicity and removal per-

1. Introduction Microalgae-based technology has also been introduced to treat

20 antibiotics. The same algal species (P. subcapitata) is even more

tions in WWTPs efﬂuents are several orders of magnitudes lower

Amoxicillin 1.34 (V€

L. Leng et al. / Chemosphere 238 (2020) 124680

L. Leng et al. / Chemosphere 238 (2020) 124680

4.1. Adsorption 4.2. Accumulation

Fig. 2. Antibiotic degradation and detoxiﬁcation mechanisms by microalgae.

4.3. Biodegradation can be treated as a two-phase enzymatic catalysis process. In the

The break-down of some antibiotics can also be accomplished

5. Integration of microalgae-based antibiotic removal with

5.2. Advanced oxidation processes

Advanced oxidation processes (AOPs) have been developed as a

other substances make the microalgae removal process more Acknowledgments

stabilization ponds. Water Res. 28, 1031e1038. https://doi.org/10.1016/0043- j.chemosphere.2017.07.085.

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