vironment Incemationa 155 (2021) 105594 Contents lists available at ScienceDirect Environment International ELSEVIER journal homepage: wor.elsevier-comilocatelenvint Review article ® Microalgae-based technology for antibiotics removal: From mechanisms to application of innovational hybrid systems Qian Xiong, Li-Xin Hu, You-Sheng Liu", Jian-Liang Zhao, Liang-Ying He, Guang-Guo Ying SU Enel Reece, OurgongPoincl Ky Labrtey of Cel Plain an Eine Sey & MOE Re ahora of Toe ‘Ohio Etro Suh Chine ermal Dae, eng 510008, Chin ‘Schon of moment, Sth Chins arma Univ Unies Town Guamgne 510006, Chine ARTICLE INFO apsTRact Heading Eton Guo pig Shere |Anibiotis contamination is an emerging environmental concern, owing ols potential isk to eeonytems and thunan bath, Mlcoalga-based technology hasbeen widely reported asa prnlsing alternative vo conventional wastewater treatment, since it i 4 solar power drives, ecologically friendly, cost effective, and sana feclanation stategy. This review provides foment insights into the major mechanisns waderpinning Imjroalgae-based antibiois removal, cluding boadsorption,bioaccunnlaton, and biodegradation. The cit eal ole of exuaclllar polymere substances on bioasorpion and extracellular biodegradation of ania fe ls covered. Moveover, ths evew sheds ight on te inpovtant factors affecting the etnoval of atibloics by miewalgae, and sunmavzes several novel appisaces to improve the removal efcienc iacuding acl ‘mation, cometaboliem and microbial consort, Hesids, hyd systems (sich ms, mitealgae-based eco: ges combined with the conventional activated huge, advanced exidation processes, constructed wetlands, an Inlroblal fuel ces), and genetic engineering ate also Zecommended, which will be feasible for enhanced removal of antbiecs. Finally, this review also highligh the need for futher studies aimed at optimizing ‘miroalgae-based technology, with emphasis on inpoving evformance and expanding its aplication in large ‘eale sting, especially in teris of technical, environmental fendy and economically compertveness, COveal chis review summarizes eutent undesstanding an mieioalgae-based technologies fr enoval of at ores and autlines fate eseich divections, eyed Imporenel bud stems 1. Introduction tons, between 2010 and 2030 (Van Boccke! er a. 2015). Among the 228 coumtries investigated in the study, China was the leading consumer, followed by the Un Boeckel et al., 2015). However, mals whieh ean be merabo- lized or absorbed necosnt for a smal fraetion, and approximately 50-90 Antibiotics ase substances with antibacterial, anti-fungal, or ant parasitica setivity, which are extensively used in huntans and animals for prevention and creatment of infectious senses, as well as in live stork industries for growth promotion purposes (Kummerer, 2009), Previous studies have reported that antibiotics consumption (data front 176 countries expressed in defined daily dese (DDD) increased by 65% from 21.1 1934.8 billion DDDs between 2000 ad 2015, whereas daily ‘consumption rate increased by 399% from 11.8 0 15.7 DDDs per 1000 Inhabitants (Klein el, 2018). Based on the eurent consumption rates, ‘antibiotics consumption might increase to 200% in 2020, if no policy ‘changes are put in place (Klein etal, 2018). Additionally, antibioties ‘consumption in livestock production evaluated with Bayesian statistical models is projected to inerease by 67%, from 63,151 tons to 105,596 percent of them are excreted via urine and feces as a mixture of parent tnd metabolite forms (Kunmerer, 200%). Consequently, released ant biotcs and their metabolites subsequently enter into surrounding en- vironments through multiple pathways, including wastewater treatment plants (WWTPS), rioft from leds into surface waters, hospitals, lve stock farms, aquaculture farms, and pharmaceutical industries [Numerous groups of antibiotics have been frequently detected in the eflients of municipal WWTPs, secondary sludge and biosolids, suxFace water, roundvaer, drinking water, and sol and sediments, with com ‘ontrosions ranging from ng/L. oyag/L level in water and ug/g to mg/kg * Couresponding aubors at: SCNU Environmental Reseach Insitute, Guangdong Provincial Rey Laboratory of Chemical Poiluion and Environmental Safety & MOE Key Laboratory of Theoretical Chenist of Envsoameat, South Cina Nodal Univesity, Gusngahou 610006, china, ‘Email addres: yousheng gins eaten (FS. Lt, guano iaga@.scs.edien (6-6. Ying). ps /door/ 10.2016 envi. 2021.106504 Received 26 February 2021; Received in eve form 19 Apul 2021; Accepted 21 Api 2021 Available online 30 Apel 2021 (0160-41207 2021 The Authous) Published by Ehevier Ud. This is an open access atte under the CC BY-NCND licensemag ea level in sediments (Huang et al, 2020; Oberoi etal, 2019; Su et al, 2018; Tran etal, 2016, 2018; Yang e€ al, 2018; Zang et a, 2019) Antibiotics contamination has gained increasing attention in recent ‘year, owing fo potential harmful risks posed by their residues tothe ‘environment and human health. Although relatively low concentrations ‘wre observed for most antibiotic residues in the environment, mounting evidences have demonstrated that they could induce adverse ‘ecological effects on target-and non target organist, such asialibiting the grovth of mietobes, altering microbial community composition and activites Gonzalez Peter et al, 2013; Huang et a, 2020; Kumar eta, 2019). Meanwhile, overuse and misuse of antibiotes could promote development and spread of autbiotic resistant bacteria (ARB) and tibiotic resistant genes (ARGS), cTeating a stong selection pressure om human and natural mierobial systems (Ashbolt ec al, 2013; He etal. 2016; Ving etal, 2017). Moreover, antimicrobial resistance has been characterized as a serious clinical and public heath issue by the frst, slobal report of World Health Organization (WHO) in 2014 (WHO, 2014), Concerus to Inman health incuded the following: (1) antibiotic resides ingested might alter the composition of Inman satestinal microbionie aad inde the emergence of ARB persisting én hniminn Dov, chen further develop into human antibiotic resistance which will, cause various diseases and even death; (2) antibiotic residues in the fenvironnient could create selection pressure on he environmental ticrobiome, and generate environmental ARB and ARGS, commonly known as environniental antibiotic resistance, which might be erans- ferred to humans relying on pathogenic ARB or human commensal ARB (shbolt etal, 2013; Ben et al, 2019; Qiao et al, 2018). Therefore, itis ‘rvieally important to conteol the environniental spread of antibiotics, ‘especially for WWTPs, where provide suitable conditions for prolife. dating of ARB or transferring of ARG. However, conventional WWTPs are not currently designed to suf ciently remove some antibities (Ahmed otal, 2017; Tran tal, 2016), In fact, they also act as major sonrces of releasing anibieies Inco the ‘environment (Zhang etl, 2015). To date, various techniques, inluding physical, chemicel and biological treatment, have been developed for the removal of antibiotes (Ahmed et al 2017; Michael et aly, 2019). ‘Among them, advanced oxidation proceses (AOPS), characterized with ‘rong oxidation capability and fast reaction rates, are demonstrated (0 be relarively effective in the removal of andbioties. However, high ‘operational and maintenance costs have limited their utilization in large-scale applications (Wang and Zhuen, 2020). Antibioties removal by physical treatment can be accomplished using powdered. or ‘granular activated sorbent carbon, where antibiotics are removed by ‘adsorption through phase-by phase separation instead of mineralizn ‘on, and che removal efficiency is significantly affected by background organic matter (Zievschmann et al, 2016). Biological treatment re mains the foundation of WWTP, owing to Its superiority to chemical ‘and physical approaches, Common biologial treatment, stich a6 aet ‘vated shidge treatment is usually incomplete, although bioremediation by pute bacteria isolated from aetivated sludge nay enhance antibiotics removal (Wang aud Wang, 2018). The main concern associated with these approaches relates 10 the potential for bacteria to develop ant Diotie resistance and transfer ARGS (Ashbolt etal, 2013; Ben et al, 2019; Qiao et al, 2018). Given the current overuse and misuse of ant. Diowes, coupled with thelr recaletrance in the environment, bio ‘magnification in the food web, as well as potential adverse effects on ‘ecorystents and human health, there is an urgent need for development ‘of novel eosceffetive mitigation technologies for removal ofa variety of ‘antibiotics, aross a range of industrial scales Recently, microalgae based technology has gained scientife atten tion for wastewater treatment, with several advantages such as being driven by solarenergy, efcent fhation of CO, eo frendliness, 48 well, ‘a being a potential feedstock for bioenergy prodvetion or orher high value-added products (Leng et al., 2020; Nguyen etal, 20208; Suther land and Ralph, 2019; Xiong et als, 2028), Moreover it guarantes cost effective remediation of various sutrients (Wong et al, 2016), seman inurl 1552021) 08504 emerging contaminants (ECs) (Sutherland and Ralph, 2019), and heavy metals in wastewater (Zeraatkar et al, 2016). Generally, microalgae exhibit great flexibility to survive and thrive in extreme environments, Wwhfeh makes thea promising candidates for enhanced. wastewater In this study, current status of research activities and perspectives the applications of microalgae based technology in reatoval of anti tes from wastewater are comprelensively reviewed. Specifically, his review provides an in-depth description of the potential mechanisms involved in microalgae based antibiotics removal, and recommends several novel approaches and hybrid techniques that ean be employed to promote the removal effic iboties and Improve practical feasibility of miroalgae based technology for wastewater teatent. ‘oalgal removal mechanisms Previous studies demonstrated that the removal of nubioties caused directly by microalgae muinly include biondsorption, bioaccumulation, tnd biodegradation (HHena ct al., 2021; Leng et al, 20207 Xiong et al. 2018), Additionally, some antibiotes can be further indirecdly removed ‘and volatilization, with the presence of micro system itself (Sutherland and Ralph, 2019). However, photodegradation and volatilization occurs under special conditions, which is wot common and wsually considered negli sible (Vguyen eta, 20208). Therefore, this review mainly focuses on the underlying mechanisms of antibiotics removed caused by bi adsorption, bioaccumulation, and biodegradation (Fig. 1). Moreover, this process can be separated into dhree steps: 1) a rapid passive adsorption via physicochemical interactions becween dhe eell surface tnd polkitants, fllowed by 2) a comparatively slow transfer of mole cules through the cell membrane, and 3) ending up with either bio accumulation, biodegradation, of both in cell (Vu et al, 2017), A Aetaled description of these removal mechanisms ate dseussed below 2.1, Bioadsorpion Bioadsomption occurs when antibioties are either absorbed into cell, wall of micronlgae, or onto organic substances, such as extracellular polymeric substances (EPS), excreted by microalgae into their sur rounding environments (Fomina and Gadd, 2014; Sutherland and Ralph, 2019; Xioug etal, 2018). EPS are mixture of high moleeular weight polymers from microorganisms, that comprise proteins (PN), poly saccharides (PS), nucleic acids, lipids, and humle substances, generally protecting cells from harsh environment (sheng et al, 2010). Microor- ‘anisms teu to excrete more EPS as an adaptlve mec in response {o antiioties toxicity (Wang ot al., 2018). EPS ean be eatogorized into ‘neo forms: ound EPS are closely attaehed to microalgal eels, while soluble EPS are excreted by microalgae in suspension or weakly attach with cells (Nielsen and Jahn, 1999). Due to their complex and diverse composition, EPS contribute t© different functional groups such as carboxy], amine, hydroxyl, and hydrophobic regions, thereby providing available binding sites for the adsorption of diverse organic and inor ganle compounds (Hansa et a, 2016; More etal, 2014), The inter action betseen antibiotics and mieroalga cell wall or excretions (both colletvely termed el surfaces is passive and non metabolic process. Functionally, biondsorption is mainly achieved through adsorption re tctions, fon exchange reactions, surface complexation reactions, chela ‘don and miero- precipitation (Ahmed eta, 2015; Tan etal, 2015), Owing to the increasing awareness of antibiotic comaninants, there huss been an inereasing in the number of published studies on the femoval of antibiotics mediated by microalgae. Related stidies have been summarized in Table 1, where naicroalgal species, expevimental setup conditions and posible antibiotics removal mechanisms ate iste. As shown in Table 1, bieadsorption is found to be one of the ticchanisnis for removal of some antibiotics, and the reported bio adsorption capacities of mieroalgse are variable, Tc was observed thatmag ea seman inurl 1552021) 08504 Extracellular biodegradato ¥ Bound EPS (attached to cell wal) Biondsorption “Soluble EPS (excreted in medium) Extracellular biodegradation Intermediate products Bioadsorption, bioaccumulation and intracellular biodegradation, Pase Ost, teucton or yates teats; ~O4 D-= Pha HCojgton ydropbobicsy of anuioies; DBondsorpion —Fametinal groups: os = «hag ten pcm ET Lettered Fig. 1. Mechanisns involved in the removal of antibiotic by microalgae ‘adsorption of 7 amino cephalosporanic acid was quite rapid initially in 10 min, with adsorption capacities of 4.74, 3.09 and 2.95 mg/g for Chlorella sp., Chlamydomonas sp. ad Mychonastes sp, respectively (iio ‘tal, 2016). Iv addition, the maximns adsorption capacities of Scene deans quadricauda and Terasebnissueciea for tetracycline were found ro bbe 295.34 and 56.25 mg/g, respectively (Daneshivar etal, 2018). These results indicated that bioadsotption capacities of mleroalgae were highly specifteto ther physical and chemical properties, such as surface ‘chemistry and surface area (Norvll et al, 2016). The cell walls of microalgae and EPS aainly eatry negative charges, de tothe presence ‘of dominant functional groups inluding carboxyl, hydroxy, and phos phoryl (Sheng etal, 2010; Xioug t al, 2018). Henee, antbiotes with Positive charge ean be effecrively adsorbed through electrostatic in teractions (xing et al, 2018). Furthermore, microalgee-mediated bioadsorption retes of antibiotics, Ihave been shown fo range fom 0 10 10086, as summarized in Table 1 For example, aitheoniyein was effectively removed by Chiorlla sac charopila (nearly 100%), whereas the bioadsorption rate of timetho prim was less than 30% (Gojkovie et al, 2018), Previous studies have ‘own thatthe adsorption performance varies, based on hydrophilicity, simicture and functional groups of different antibioties (Hien et al, 2021; Xiong etal, 2018). Generally, ipophile compounds have high biondsorption affinity valies to micronlgae due to electrostatic in teractions, while hydrophilic compounds exhibit low bioadsonption af finties and are more persistent in growth medium (Sutherland and Ralph, 2019; Xiong et, 2018). The ipophilieity or hydrophobiciyy of a substance can be evaluated in teris of og Ko (Oetanol-waterpartcion coefficient), with a higher log Koy value implying elevated edsorption of ‘compounds onto the surface of microorganisms of the solid phase (Covdeet, 2008). Antibiotics with high log Koy values (5) and high molecular weights tend to be easly adsorbed than those with [ow log Koy Vales (<2.5) (Tiwari et al, 2017). Mareover, Wells (2006) sug _gested that log D, a solid-water distribution coefficient of compounds at ‘given pH can also be applied to assess sorption mechanisms alongside hydrophobicity. Previous studies demonstrated that the removal eff leney of trace organic compounds with og D > 3.2 devoted by bio ‘adsorption was over 85%, whereas for those with log D < 3.2 were less than 20% (Tadkaew et al, 2011) Since bioadsorption is a now metabolic proces, binding of antbi totes onto the mieroelgal surface aceurs on both living and non-living ‘uicroalgal cell surfaces, and the biomass of non-living microalgae has been proved to be a great potential biosorbent for the removal of ant bioies In modeling wastewater, cefalexin (#90 mg/L) was effectively removed by nonliving Chlorella sp. and lipié extracted Chlorella sp, with sorption capacities of 129 and 63 mg/g, respectively (Angulo ea 2018). Additionally, Daneshvar et al. (2018) obained «maximum ‘sorption capacity of 295 mg/g removal of tetracycline from water by lipid extracted Scenedesmus quadricauda, Generally, non-living micro algal biomass applied as bioadsorption agents have several advantages ver living microalgae, such as no toxieity limitations, improved sus tainabilty of algal biodiesel in an environnuentalyfrendly manner, and reduction of operational costs (Nautiyal et al, 2017), Although io- adsorption provides an alternative treatment option for some anti ‘ates, further studies are needed 1o improve the engineering feasibility of tmeroalgalbioaésorption technologies. ‘Microslgae-based bioadsorption is highly dependent on the stnctane ofthe target antibiotic (eh as its hydrophobicity and functional groups available for chemisorption), micronlgal species acting as sorbent, ad fnvironmental conditions (Noril ta, 2016). To improve microalgal adsorption cehiologies in bioremediation, several approaches, sich as bioprospecting for species with a high affinity for dhe target antiioti, and preferentially adsorbing it onto the cell surface, have been pro: posed. Consequently, microalgae from Chlamydomonas, Chlorella and ‘Scenedesmus genera have been identified, and are che most frequently used species for antbiote bioremediation owing co their availability and reat potential (Sutherland and Ralph, 2019). Hyper-adsorbency by the mjcroalgae can be achieved by optimising variables that influence the bioadsorption process, including biosorbent dosage, initial adsorbate concentration, contact tine, pH and temperature, as wells stimulation of EPS exeretions (Sutherland and Ralph, 2019). For example, the removal efficiency of metronidazole by Chlorella vulgaris decreased with increasing initial concentration of antibiotics (Hens et aly, 2020) ‘Tetracycline biondsorption by Scenedesmus quadricauda dramatically Increased during @ 60 min period, whereas fs removal by Tetraselnis suecica was not time-dependent (Danesivar etal, 2018). Moreover, bioadsorption is a pH-dependent process, where pH affects bothmag ea Removal efficiencies and main mechanisms for @ range of antibiotics by ‘Table 1 mlerwalgae. nubioie compound Mioaal pecs (stl enatone senor eflney ‘id calase ce) amine hot. ce eplalmoranie 01 00mg, wa 758,338 hime fp tae 00 mp 738,15, (Siphon spi (too meh 75h. 13 a prewir (40 wel 96h 240° Arosa Mires cara (00. nasi, 74" plot 20 8. 7a 40 8 ‘eprom 20 fetarm 00 Stoedom ‘peed 20 fer 62s, 28, Chet vas (ab pet 385 20 a copttena ering Clo sp (s0202 mp ery (cbnined Nomar ser pt ‘reaction! 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Smlome rewire nace 29 ‘eum eae fees 00", asp (ms ‘hire ier asae (cope 20 Sulimeduane Crea a 9G11.45-59nodepataton ar. there i7mis ysl anderen rad ot drei SV Semedamay” 25,20 mL cet signet ae, wa oh ton isar Shee Not deemed Chore Paawl —dotepnsaon Serine 20 et, 90 proline 10 ie pene 267° eine MeLeS0K19 im, 2000 Bonewmean Se toot “ hae Note: BG11(Blue-Green medium), BBM (Bold's Basal Medium) Saneesne acces reseried degradation ME et al, 2016), Shu ta, 2017), Lt a, 2015), “Kil ea, 2020, oie, Seu Stange a, 2018), Che et a, 2015), 7 ea, 20200, ong eal, 20174}, MChen et ak, 2020), “Xiong etal, 20170), "(Sang et a, 2010),mag ea Foxiong et al, 2017) "lena ef al, 2020), M(Gojhovie ea, 2019), csanteuteia et al, 2016), Ba and Acharya, 2016), "™StavseC a, 2017), *¢kiong et al2020), sun eta, 2017), "(Nov et a, 2017), *"Danesear ec al, 2018), (de Goose al, 2012), de Wil et al, 2016) Ionization or dissociation of antibiotics in aqueous media, as well as surface charge of biosorbents (Daneshvar etal, 2018). Apart fom these factors, bioadsorption is» chermodynamie process where alterations in emperanire have been shown to affect the rte of atiiotes ndsorpcion ‘on the microalgal cell surface Zeraatkar et al, 2016). The quantity and ‘composition of EPS aso reportedly afects antibiotics sorption, with a higher PN/? (proteins/polysacelaries) ratio in EPS implying stronger hhydtophobieity and more adsorption sites (Sheng et al, 2010). 2.2, Bioaccumulation Bioncenmalation is mn active metabolic process for uptake of ant bioties in living microalgal cells, where they bind to intrcelisar peo teins or other compounds (Xiong eal, 2018). Although biondsorption is ccotsidered as the first step of bioaccumulation, not all pollutants adsorbed onto che surface of microalgae can enter Into dhe ell t0 bo ‘accumulate (Wu etal, 2012). Antibioties ean be transported across the microalgal cll membrane ito the ell via three major pathways: (1) passive diffusion, (2) passive-frclitated difision, and (3) energy dependent/active uptake (Sutherland and Ralph, 2019). Passive dif ‘ion of antibioties requires no energy, since some antibiotes ean dfse trough the cell membrane from a region oF high (external) co low (i temal) concentration, Antibiotics with love molectlar weight, especially non-polar and lip soluble ones, might pass chrough the cell membrane via passive diffusion due to its hydrophobicity. Bioaccumulation was previously observed during removal of trimethoprim, slfamiethoxszole, florfenicol and carbamazepine, where antibiotics entered into micro ‘algal cells via passive diffusion (Bal and Acharya, 2017; Song et l., 201%; Xiong eal, 2016), Additionally, alterations in the permeability oF the cell membrane induced by tne exposure of antibiotes or stress ‘environment ean aso cause passive diffusion, a phenomenon that is attributed 10 membrane depolarization or hyperpolarization (Suther land ond Ralph, 2019). Interference with the integrity of the cell ‘membrane may also promote passive diffusion of antibiotics. For ‘example, ation of 19 (w/) sodium chloride significantly improved bicaccunulation of levofloxacin by Chlorella vulgaris ro 101 ug/g, while those without sodium chloride was 94 yp/ Cilong et al, 20178) Passive faelitated difasion means that antibiotics move aeross the cell ‘membrane with the help of transporter proteins, whose role is to mediate influx of polar moteetles into the cell. The third pathway refers to an active transport process driven by energy, where antbioties move ‘against a concentration gradient (Sutherland aid Ralph, 2019) Bioaccumulation is influenced by external and internal physico ‘chemical environments, including temperature, pH, contact time and Wibiotic concentrations. For example, temperature was shown (0 significantly affer biowectnlation of antibioties i the planktonte food ‘web (Fang etal, 2020). Specifically, the bioaccumulation factor of sn UUbjotics increased withthe mean temperature only at lower tenipers tues, but decreased with the mean temperature when it was higher than 195°C, 21.5°C for phytoplankton and zooplankton, respectively CPaig ‘tal, 2020). On the other hand, bioaccumulation of carbamazepine in Cchlanydornonas mexicana and Scenedesmus abliquue increased with in crease in catbamazepine concentration aad cultivation time Oxon, ct al, 2016). Sinilany, wieh the increase ofits initial concentration in the medium, part of florfenicol might be absorbed by Chlorella sp. £38 Ciasorption) and migrated into mieroalgae cell (bionecumalation) (Gong el, 2019). Optimization of those physicochemical parameters may affect both the rate and quantity of antiboties accumulated by microalgae, and protect the cells from any associated toxicity, thereby. promoting antibiotics removal. In addition, several recent studies have been conducted to sereen micronlgal species that are both tolerant co seman inurl 1552021) 08504 nticipated concentrations of antibiotics and confer high bio: accumulation rates (Gojkovic etal, 2019; Sutherland and Ralph, 2019). Since biondsorption represents the first step of bioaccumlation, ant bioxies aecumularing in cells must fulfill the necessary Key criteria for biondsorption. However, not all antibiotics adsorbed on microalgel surface can accumulate in cells (Wu etal, 2012). Moreover, the accumulated antibiotics in mieroalgal cells might stimulate overproduction of reactive oxygen species (ROS), ineluding free radical (superoxide radical (03), iydroxpl radical COFD, perhy” droxyl radial (#102) and alkoxy radicals), nonradiel frmis (hydrogen peroxide (H,0,), and singlet oxygen (403) (Karade etal, 2016; Xiong , protons and electrons in the anode pole. Then electrons are transferred through an external circuit co the cathode pole, whilst the protons migrate from anode to cathode through electrolyte (salt ridge or iembrane separators), Finally, terminal electron acceptor, sch a, oxygen, organic pollutants er heavy metal, is reduced in the eathode pole after accepting electrons and protons (Nogendranatha Reddy ec a. 2019; Sab eal, 2017). Previous studies have demonstrated that MFCS can efficiently remove organic matters within a reasonable hydraulic retention time, although they axe restricted to the removal of nutrients due to anaerobic condition inthe anodie pole Hassan etal, 2021; Yan Cal, 2019). To overcome these challenges, researchers have introduced ‘microalgae ar either the anode othe eathodie conipartments of MFC ta tctas substrates for oxidation reactions under enserobic conditions of to generate oxygen for using as electron acceptors, respectively (Sabi ct al, 2017)mag ea To data variety of microalgae have been reported to integrate with MPCs for wastewater teatment, mainly including the genera Cre, Scenedesus, Microcystis and Ghlanydomonas (Bhatia et al, 2021; Shukla ‘nd Kumar 2018). A study by Ndayisengs eta. (2018) found thatthe power generation and COD removal capability of MECS fed with Clr sla regulars (MFC Algae) were comparable to those ofa commercial ‘acetate fed MCS, indicating that microalgae were suitable substrates in MFCS systems, Snilar results were reported by Ale (2020), showed thar hermafi all biomass ould aso be urlze in MFCs for sustainable ‘wastewater management and algal Boonis mitigation. Moreover, ne {rated system comprising MCS with Mieroysti aeruginosa was fond Co coupleely elininate microosin-LR, with eomperable COD removal effclency (67.5 1.0%) and higher power density (83 mW/n?), rel tive to MFCS-Aceate (Al tal, 2020). An immobilized microalgae based photonitotropiie MFCs, developed forthe rt time o sina neously eliminate nuients and recover bloenergy from domestic wastewater, exhibited excellent removal flees (Wang et, 2019). Specially, this system eliminated 93.2% of SCOD, 95.9% of NHE-N, 95.19 fT, ad 82.79 of OEP, and sw masa power density of 66.9 W/m (Wang etl, 2019). Additonal, mixed cu tures ea also be used to integeae with MFCS for wastewater eaten snd boeletricity production (Sash tal, 201; Sun el, 2020). The Injeroalgae bacteria MES has emerged a an efficent approach for suppressing anibiode contaminants, in which myrobial metabolism ‘copes with electrochemical redox reactions for efficient antibiotics removal (iassan etal 2021; Sn et al, 2020) Sun etl. (2020) ‘auployed a novel miroalgae bacteria MECs syste to simultaneously degrade anoie Moreno, elininate eathodie nitrogen and generare Uieleetriity. Moreover, some esearches belive dt MFCS system ct sso contribie tothe removal of ARB and ARGs (Yan etn, 2019). ‘Thereore,& combination of MECs technology with microalgae based proces ca inprove overall performance, achieve sustainable west tater treatment (iniropeliaants av nutrients removal couple with Tow greenhouse gases enission and reduced shidge production (alos nest etal, 2020; Nagendranathn eddy et al, 2019). In adation, this ‘pproach can ditety convert electrical energy to chemical energy, and prodice biofuels or valuable recovered material from scronlgl Biomass (Bologuest et al, 2020; Nagendranatha Reddy etal, 2019) “Taken together, these rests suggest thet the hybslé MFCs-aueroalgne process a novel alternative for wastewater treatment, which also ‘uarantees sustainable recovery of renewable energy and biologie! proves 5. Potential for genetic engineering in improving microalgac- based antibioties bioremediation Generally, microsite exhibit species specific preference and toler ‘ance to surroxnding environments, as well as speifie performance for the biodegradation of different antibiotics (Leng etal, 2020; Nguyen ‘etal, 2020c; Sutherland an Ralph, 2019). In this context, prospecting for suitable nirobial stuns isa eral fist step towards constricting a stable mieroalgse-based system for continuous end efficent removal of pollstans fom wastewater, as well a a vital factor for the sustainable ‘production of biofuels (Courtens et al, 2016; Perera eta, 2019; Zer ‘suka eta, 2016; Zhang eta, 20200). High-throughput sequencing Technique provides insight to analysis of de microbial comm stricto, functions and dynamics im the microalgae-based system, as ‘well as isolation of microbes with capacity for efficient biodegradation ‘of mieropollutans (Nguyen etal. 20200). The biodegradation capacity ‘of chloramphenicol by enriched bacteril consortium was investigated Dy Zhang eal (20201), and results indicated chat the eore bacterial genera including Sphingomonas, Cupriavidus, Burtholderia, Chrys ‘obacterum, and Pigmentiphaga. Moreover, csloramphenicol was found tobe completely removed by the isolated Spkingomonassp.CLS.1 in 48 with a mineralization rate of 50.496 (Zang et al, 20201), Besides, genetic engineetng has also been used to expt engineered, seman inurl 1552021) 08504 microbial strains or consortium, aiming at improving the specific retabolie activities of microbes or entiching microbes with specific functionality (Khatiwada ct al, 2020; Rios Miguel et al, 2020). Compared with wild-type bacteria, hermotolerant facultative angerobes modified via genetic engineering showed significantly improved eff cent degradation capacity on various nitroalkanes (Zang tal, 2021a) Microalgal cones, engineered with functional enzyme genes sch 8 lncease enzyme, were shown to improve oxidoreductases stability, guaranteeing effective bioremediation of pollutants (Si ‘stichandraose et al, 2013), Laceass are extracellular oxidoreductases that are abundant in bacteria and plants. Functionally, they ean eatayze f broad variety of reactions due to their low-substeate specifiy, especially one electron oxidation of monophenols, diphenols, and polyphegols as well as aromatic amines, diamines, among others (ill ral, 2019). In addition to being able of introducing functional genes lao ‘Imiroalgal genome, targeted genome editing is becoming increasing popular in the modification of microalgal strains (kitivads (al, 2020). CRISPR based gene targeting recology was successfully applied in Euglena gracl, achieving a glucan synthase like 2 gene responsible for paramylon synthesis (Voniira etal, 2019) Although microbes modified by genetic engineering show highly biodegradation capacity of micropollutants in Iabscale reactors, their pplication in WWTPs renains controversial. The societal concerns to wards gene modification strategies are related to the unforeseeable ef fects of microbes with new funetions in an open environment (Trump cal, 2020), Additionally, the enhanced transfer of modified genes may also accelerate the mobilization of ARGS. Therefore, further efforts should be focused on the application of genetc engineering technology 1 onsite reactors at WWTPS, and on risk assessment of gene mod tation sich as the trator of ARGs, to broaden their application in wastewater bioremediation. 6. Concluding remarks and perspectives The overview of microalgal bioremediation suggests @ promising outlook for the application of microalgae-based technology in waste Water treatment. For andbiodes, bioadsorption, bioaccumulation, and biodegradation are demonstrated to be the three major removal mech: nisms mediated by microalgae (Hena et al, 2021; Leng eta, 2020; ‘ong et aly, 2018), Additionally, ther isa strong evidence that EPS plays an important role in che bioadsorption and extracellular biodey. redation of antibiotics (Sheng et al, 2010; Xiao and Zheng, 2016) However, the role of EPS involved inthe removal of antibiotics and the lunderlying mechanisms associated with the complex interactions be tween EPS and antibiois remain unclear. Even though the biodegr ation mechanisms of antibiotics have boon widely investigated by previonsstdies, which are not fully understood, especilly at the mo: lecular level. Omies technologies, such as transeripcomics, genomics, proteomics, and metabolomics, are shedéing lights on unraveling ametional genes associated with metabolic pathways of antibiotics, ‘dontfying the potential proteins that mediate electron transport, a6 woll as enzymes that catalyze metabolic reactions of antibiaies(Mishre cal, 2019; Ularte etal, 2015). Moreover, combination of mut-omies technologies has facilitated further comprehensive understanding ofthe ‘underlying. mectanists of mietopolivants biodegradation (isis cal, 2019). Even though omics technologies have emerged as prot sing molecular tools, the application of uni-or mult-omies approaches ln wastewater bioremediation mechanisms is stil in its iafaney and critical overview of these technologies used to date is Limited Mieroalgne are emerging as highly attrsctive candidates for biote tmedlition especially in wastewater treatment, but they exhibit Knited biodegradation capacity of some recaleitant antibiotics. Several novel fpproaches are recommended in this review to improve the removal efficiency of recalcitrant antibiotics, inchuding acclimation, co: tuictabolisa and microbial consortia. Micronlgae acclimated wnder harsh or limiting conditions show higher tolerance and biodegredaconmag ea ‘capacity than wild-type microalgal species (Chen etl, 2015: Liao etal, 2016; Osundeko ef al 2014; Xiong et al 2017a) However, lite is Jnown about the ability of microalgal species response to various ‘environmental stresses, and In-depth studies are needed co reveal the ‘ole of the stress conditions in improving removal of organie contami ‘nants, Previous studies have shown that co-metabolism is an effective scategy for promoting microalgae mediated biodegradation of antibi ‘tics, and the type and concentration of carbon sources play the most ‘erties role in the co-metabolie of antibiotics (Liang et a, 2019; Vo ‘et al, 20208, 202005; Xiong etal, 2018, 2020). To date, most studies focus on sereening an appropriate carbon source and optimizing its ‘concentration, while the response mechanisms of mletoalgse 0 carbon. some is not available. Besides, microm consortium applied for wastewater tentmient has boon demonstrated to be cost effective and ‘environment friendly (Goncalves et s., 2017; Lee and Lei, 2019; Lin fetal, 2017; Nguyen et l,, 20204). The Interactions established in consortium are usually elucidated from biologie and physical pe spective, limited information Is Kou about thelr inter mechanisms a the molecular and biochemical loves, 1 is essential to completely wn ders the complex and dynamic interactions involved in consortiums, ‘which constitutes a crucial frst step cowards the construction of engi ‘neered consortium for their efficent application in wastewater treat ment ad bio. products recovery. However, che application of genetic ‘engineering technology in wastewater bioremediation remains need ‘more attention, especially with respect to the risk assessment of gene ‘modification sich a8 the transfer of ARGS, On the other hand, four hybrid techniques based on microalgal treatment are recommended in this review, which are proved to be & promising approaeh for mieropollucants removal in wastewater treat ‘ment (Grandelement et al., 2017). However, most of hybrid systems and ‘above mentioned novel approaches are performed in Inboratory seale ‘units ad stil at inital stages of development, There are still challenges ‘and critical problets to expand their application in fllseale WWTPS ‘with regards to techniesl, environmental friendly and economically ‘competitiveness, Previous studies have mainly focused on improving effciency of microalgae mediated removal of antibiotics, while know ‘edge on the consequent fate of ARGS and ARB in wastewater remains limited Besides, although a andl studies have investigated toxicity of effluents after” conventional wastewater treatments, similar in ‘vestigations on hybed system are unavailable. Therefore, fate studies should seek to estimate the actual performance of hybrid system, with regards o efficiency of removal of ARGs and ARB in sition to targeted ‘anlibioies, as well asthe toxicity of effluents, Overall, given the diversiy of antibiories pollutants andthe ‘complexity of realistic pollutant environments, several challenges with respect tothe improvement of the removal capacity, revelation of inner molecular mechanisms, developinent an application of hybrid eystem ‘removal of ARGS and ARB, ns well as toxicity investigation of events ‘temain to be addressed and need more attention Declaration of Competing Interest ‘The authors declare that they have no known competing financial interest or personal relationships that could have appeared c influence the work reported in this pape: Acknowledgments ‘The authors would like to acknowledge the financial suppor fom the National Natural Science Foundation of china (U1701242, 42030703 and 41877350). The National Key Research and Development Program of China (2020¥FC1806901 ané 2020YFC1806504), Guang- dong Provincial Key Laboratory of Chemical Pollution and Environ ‘mental Safety (20198030301008), and Natural Science Foundation of ‘Guangdong Province (2020A1515110926) seman inurl 1552021) 08504 References chem, ie, asl, Yo, B, Keene, B.A, Con PE eK 2018 attra of loanie bes tn acted ls: Te ramon rn erp etme a nen Tce 32 om wot an watever Pope an linge 5 Tol Eon 552, Jn Ws Sng BP 209, Tr be a ene tvn Fls 208 157% van Nano Snr Oi Cavin PA aj 206 ae of Biowasmatn stn an milion f (16 ald sttnethowcle ne ire eon nda Sol Eon, 700 tii ing rte lsc Ba An Ns Amex be kos Tonle ran Clg, Coc, ney ase, Weber twee tiem, etn, Ri J Seon yi Pope, Ya aE, Topp 201, man et semen (aR) fr ero epee st fie eo: es Pp Se, 20s, sessment of dub soles p18 Ban haya Rae, tenval of tino, Pontoon wan ty the en as Now pat Mae 15,7075 penal (ER) am ake Mend we Se Toa aS 983 sti of eine rine send wi nto eee sa Sy bp Rt me Peed, Aa, LX ‘abn, A Waar GH, Seo 8.0, Yang Ht Waseter aed tong ener eet reer rege nd legs Tt i le oe th, bel MLK 2009 eigenen tig oct ye ington Bolan, Coe Gale A Cg, A, 202, Combet iene Bou Riko, eT Cavin, Kobe, B.A, 2012 ato of ace sans pale of ltmetbeattemraaton om an cna Pree beet ap Eton, Mobi 78 27727 Dehn eC Ge Ch ame, 1M, 2014, Mae eye Fete ‘is bc acca i ype sR hens Zhen FO RX 201, Ag fede on er ney in Teather lane pac AN) oe mite Ps Che ily Zhang Han YA, Fg Wan HL 229, Dereon sn ‘espn in nd enn elo ho, ste, Ys in Kn MH, Cha, Ys i, De at 26 Us of eed ose ss wecinstn tse a fo nto poten by te rn ral a a is Contes EM, Sk VeVi, Bobs Ste, Sean te Pp, Dt Vemich, Si, Bow M2016 A rob mtin nig in bana °C ope op hp hoc on Desa Zari, Ml, Hein, AM, Paha, Hames, A, 2018 “ute bps ltt nie at ol ey ‘ere an pi tnt nd wn ps, i de Gane Manor. 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