Bioresource Technology 222 (2016) 485–497

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Bioresource Technology

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Review Perspectives on the feasibility of using microalgae for industrial wastewater treatment

Yue Wang a, Shih-Hsin Ho a, Chieh-Lun Cheng b, Wan-Qian Guo a, Dillirani Nagarajan b, Nan-Qi Ren a, ⇑ Duu-Jong Lee a,c, Jo-Shu Chang a,b,d, a State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of Technology, Harbin, China b Department of Chemical Engineering, National Cheng Kung University, Tainan, Taiwan c Department of Chemical Engineering, National Taiwan University, Taipei, Taiwan d Research Center for Energy Technology and Strategy, National Cheng Kung University, Tainan 701, Taiwan highlights

 Four industrial wastewaters treated by microalgae-bacteria consortia were reviewed.  Photobioreactor design for wastewater treatment with microalgae were described.  Feasibility and potential of microalgae-based wastewater treatment was evaluated. article info abstract

Article history: Although microalgae can serve as an appropriate alternative feedstock for biofuel production, the high Received 4 September 2016 microalgal cultivation cost has been a major obstacle for commercializing such attempts. One of the fea- Received in revised form 25 September sible solution for cost reduction is to couple microalgal biofuel production system with wastewater treat- 2016 ment, as microalgae are known to effectively eliminate a variety of nutrients/pollutants in wastewater, Accepted 26 September 2016 such as nitrogen/phosphate, organic carbons, VFAs, pharmaceutical compounds, textile dye compounds, Available online 13 October 2016 and heavy metals. This review aims to critically discuss the feasibility of microalgae-based wastewater treatment, including the strategies for strain selection, the effect of wastewater types, photobioreactor Keywords: design, economic feasibility assessment, and other key issues that influence the treatment performance. Microalgae Algae-bacteria consortium The potential of microalgae-bacteria consortium for treatment of industrial wastewaters is also dis- Wastewater treatment cussed. This review provides useful information for developing an integrated wastewater treatment with Photobioreactor microalgal biomass and biofuel production facilities and establishing efficient co-cultivation for microal- gae and bacteria in such systems. Ó 2016 Elsevier Ltd. All rights reserved.

Contents

1. Introduction ...... 486 2. Selection of microalgae species used in wastewater treatment ...... 487 3. Potential of algae-bacteria consortium system used for wastewater treatment ...... 488 4. Biological treatments of different wastewaters using microalgal cultures ...... 491 4.1. Pharmaceutical wastewater ...... 491 4.2. Dye-containing wastewater ...... 492 4.3. Metal-containing wastewater...... 493 4.4. Agro-industrial wastewater ...... 493 5. Photobioreactor design for microalgae-based wastewater treatment...... 494 6. Conclusions...... 495

⇑ Corresponding author at: Department of Chemical Engineering, National Cheng Kung University, Tainan, Taiwan. E-mail address: [email protected] (J.-S. Chang). http://dx.doi.org/10.1016/j.biortech.2016.09.106 0960-8524/Ó 2016 Elsevier Ltd. All rights reserved. 486 Y. Wang et al. / Bioresource Technology 222 (2016) 485–497

Acknowledgements ...... 495 References ...... 495

1. Introduction hinders the use of microalgae as biofuel producer. Some scientists demonstrated that algae cultivation using various wastewaters is a Global carbon emissions are expected to increase from the cur- more effective and economic way to reduce the biomass produc- rent 404 ppm of atmospheric CO2, along with severe environmen- tion cost, and notably, providing the extra benefits of simultaneous tal issues. Algae are an effective intermediary which can convert wastewater treatment (Wang and Lan, 2011; Wang et al., 2015b; carbon dioxide and solar energy into various bio-energy forms Wilkie and Mulbry, 2002). It has been reported that some microal- (such as biodiesel, bio-ethanol, and bio-butanol), since they pos- gae can simultaneously remove nitrogen and phosphorus from sess 20% higher photosynthetic efficiency compared to terrestrial domestic wastewater down to very low concentrations of plants. However, currently, the worldwide production of microal- 2.2 mg LÀ1 and 0.15 mg LÀ1, respectively, by uptake of the nutri- gal biomass is only about 9000 tons yÀ1. More importantly, the ents into the cells (Boelee et al., 2011). Until now, microalgae is production cost is as high as $20–$200 kgÀ1, which significantly most commonly used for the treatment of municipal wastewater

Fig. 1. COD/nutrient removal using of microalgae-bacteria system, (a) integrated processes, (b) nutrient and energy flow in microalgae-bacteria consortium. Y. Wang et al. / Bioresource Technology 222 (2016) 485–497 487 and concomitant biomass production. Some high-COD and ter treatment to avoid the external oxygen supply, allow nutrients nutrient-rich wastewaters, such as industrial and agriculture assimilation into biomass, and reduce CO2 emissions to the atmo- wastewaters are usually combined with anaerobic pretreatment sphere. Particles of senescent and dead algal materials are sources or diluted appropriately to avoid algal growth inhibition caused of organic compounds that are liberated as Dissolved Organic Mat- by the high COD concentrations (Wang et al., 2015b). In recent ter (DOM) by aggregate associated bacteria. Nevertheless, the days, an increased number of studies on industry wastewater implementation of an integrated algal-bacteria system faces chal- treatment by microalgae are also successfully conducted, such as lenges as well. For examples: (1) Little is known about the complex sugar mill effluent, pulp and paper industry effluent (Polishchuk tripartite interactions between algae, their associated microbial et al., 2015), fish farm wastewater, coal-fired metal-contaminated consortia and wastewater associated microbes for the growth wastewater, petroleum industrial wastewater, pharmaceutical and utilization stages of the biofuel algae, leading to difficulties industry wastewater, textile dye industry effluent, and electroplat- in creating a stable co-cultivation system. (2) Phytoplankton- ing industry wastewater. Notably, both photobioreactors and bacteria interactions can range from symbiotic to parasitic, with wastewater treatment plants (such as oxidation ponds) can be algae inhibiting or benefitting bacteria, and bacteria inhibiting or employed for microalgal biomass production and simultaneous benefiting algae, depending on the bacteria and algae that are pre- wastewater treatment. High rate algal ponds (HRAPs) and oxida- sent in the co-culture system. In addition, microalgae is an effec- tion ponds are the most employed wastewater treatment plants tive platform for promoting electron and energy flow in a for both municipal and industrial wastewater treatment combined microalgal-bacteria symbiosis (Fig.1). with microalgal biomass production. Considering the above men- tioned factors, the high potential of microalgal wastewater treat- ment process is clearly demonstrated (Fig. 1). However, few studies reported that the algae organic matters 2. Selection of microalgae species used in wastewater treatment (AOM) secreted during algal growth would form various odor and taste compounds, which will adversely affect the effluent qual- Using microalgal cultivation as a tertiary wastewater treatment ity after algal growth (Wang et al., 2015b). Odor is an index to eval- process started since 1970 s. The most desired characteristics of uate the quality of effluent from wastewater treatment plant, and algae for the use in wastewater treatment and biofuel production these compounds can increase the COD of effluent. This is disad- include higher growth rate, high lipid content and productivity, vantageous, as the primary aim of wastewater treatment is to higher tolerance to the possible pollutants – metal ions and toxic + reduce COD and other organic nutritional compounds in the efflu- compounds present in the treated wastewater, high NH4 tolerance, ent. Compared to the conventional activated sludge based wastew- high O2 generation rates, high CO2 sinking capacity, and robust ater treatment, several obstacles in microalgae-based wastewater growth properties with improved tolerance for varied environmen- treatment systems often exist: (1) The COD loading (F/M) is lower tal conditions. These criteria are of prime importance and algal for algal treatment processes, whereas activated sludge process growth has been reported as the limiting factor in nutrient and pol- can treat wastewaters with a wider COD range. For instance, algae lutant removal efficiency of an algae-bacteria consortium. The can grow well only in wastewater containing lower COD (below selection of microalgae for a particular treatment option can be 5000 mg LÀ1)(He et al., 2013; Wang et al., 2015b). (2) The extracel- based on the knowledge about the indigenous species in such lular organic matters produced during algal cultivation may wastewaters, making use of their characteristics for our advantage. increase the COD of wastewater (Wang et al., 2015b). In general, Several microalgal species (such as Chlorella sp. (Wang et al., the COD of wastewater will be consumed effectively in the first 2015b), Scenedesmus sp. or Desmodesmus sp. (Ji et al., 2014; several days, but in batch mode processes, the excess extracellular Martinez et al., 2000), Neochloris sp., Chlamydomonas sp. (Xiong organic matters may accumulate with prolonged cultivation time, et al., 2016), Nitzschia sp., and Cosmarium sp. (Daneshvar et al., resulting in a possible increase in the COD level (Wang et al., 2007)) have been applied for various types of wastewater treat- 2015b). Thus, part of the microalgal biomass should be harvested ments coupled with biofuels production under sterilized or non- in time, to avoid the production of excess extracellular organic sterilized conditions (Fig. 2). Among them, species of the genera matters. Most microalgae require longer period to accumulate Chlorella, Scenedesmus, and some cyanobacteria are the most huge amounts of lipid or carbohydrate (i.e., used for biofuel pro- employed species in various wastewater treatments due to their duction) and the risk of pollution and ecological hazards caused high growth rate, high environmental tolerance, and high lipid/ by the AOM will significantly increase. (3) When wastewater starch accumulation potential (Kim et al., 2016; Wang et al., sources are located in areas with extreme environmental condi- 2015b). For instance, Chlorella sp. is widely applied in the wastew- tions, either high altitude hypothermic area with low insolation ater treatment because of its enhanced ability in removing nitro- (Talbot et al., 1991) or low altitude high temperature region with gen, phosphorus, and chemical oxygen demand (COD), while high insolation, selection of an algae that can proliferate under Scenedesmus sp. can be cultivated in high saline piggery wastewa- harsh environmental conditions is of paramount importance. How- ter (Kim et al., 2016) and high COD-loading swine wastewater ever, most microalgae species can only grow well within the range (Prandini et al., 2016). Zhou et al. (2011) isolated microalgal strains of 25–35 °C, which will limit the use of microalgal wastewater from various wastewater treatment sites and found that five treatment in practice (Ruiz-Martinez et al., 2015). strains (of the genera Chlorella sp., Hindakia sp., Scenedesmus sp., Taking these into account, development of algae-bacteria and Auxenochlorella protothecoides) had higher biomass and lipid consortium system may be an ideal process to solve the above- productivity. Of those, Scenedesmus sp. had a biomass productivity mentioned obstacles associated with microalgae-based wastewa- of 247 mg LÀ1 dÀ1 with 30% lipids per dry weight. In another study, ter treatment process. The AOM can help promote bacteria zooglea when grown in municipal wastewater, a Scenedesmus sp. strain had formation in some cases since the AOM mainly appeared as a biomass productivity of 132.4 mg LÀ1 dÀ1 with a lipid content of polysaccharides. In the co-cultivation system, the conventional 11.04% w/v (McGinn et al., 2012). Oil mill effluent was also used for activated sludge with bacteria can effectively remove the organic the culture of Scenedesmus sp. Since the effluent caused darkening carbon source (COD), along with the generation of CO2. Through of the medium, heterotrophic growth of Scenedesmus sp. was À1 À1 photosynthesis, algae can convert CO2 to biomass and produce observed with a biomass productivity of 120 mg L d and a lipid À1 À1 O2 to support the bacterial growth (Fig. 1). Thus, the algae- and carbohydrate content of 164 mg L and 174 mg L , respec- bacteria consortium system can be perfectly applied for wastewa- tively (Di Caprio et al., 2015). 488 Y. Wang et al. / Bioresource Technology 222 (2016) 485–497

vlgaris Cyanobacteria sorokiniana Municipal wastewater Chlorella Fish farm wastewater pyrenoidosa Chlamydomonas Arficial wastewater minussima slaughterhouse wastewater Cosmarium kessleri Anaerobic digeson effluent Desmodesmus livestock wastewater Chlorophyta protothecoide Texle dyes wastewater Ankistrodesmus zofingiensis Swine industry wastewater obliquus Scenedesmus dimorphus Pharmaceucal wastewater dairy wastewater acutus Dunaliella platensis Agro-industrial wastewater soybean processing wastewater quadricauda electroplang wastewater Neochloris oleoabundans Metal containing wastewater pseudoalveolaris coal-fired waste water Bacillariophyta Nitzschia Industrial effluent(ethanol Euglenophyta Euglena and citric acid producon) Macroalgae Lemna minuscula Sargassum Sugar mill effluent Pelvea canaliculata Ascophyllum Fucus spiralis Laminaria hyperborea Oedogonium

Fig. 2. Microalgal species used in various wastewater treatment.

Botyrococcus braunii, a green freshwater microalga, is known for 3. Potential of algae-bacteria consortium system used for its unique ability to constitutively synthesize and store high quan- wastewater treatment tities of a wide variety of lipids (Tanabe et al., 2012). Chinnasamy et al. used carpet industry wastewater as a nutrient source for It has been observed that the co-cultivation of algae and bacte- À À growing B. braunii and a biomass of 340.4 mg L 1 d 1 and a lipid ria can stimulate algal growth; algae and bacteria are widely productivity of 13% DW was obtained (Chinnasamy et al., 2010a, known to form consortia in nature. The symbiotic association of b). It is worth noting that the lipid production obtained from the algae and bacteria in an algae-bacteria consortium is summarized axenic culture of B. braunii is equivalent to oil production associ- in Table 1. Some researchers pointed out that even the axenic sta- ated with the consortium of five microalgal strains and the esti- tus of laboratory microalgal cultures is questionable. Park et al. mated oil yield from biomass produced with untreated (2008) isolated eight bacterial strains from a laboratory stock of À À À À wastewater were 3675 L ha 1 yr 1 and 3830 L ha 1 yr 1, respec- Chlorella ellipsoidia and found that a single bacterium Brevundi- tively, for B. braunii and the consortium. Although B. brauni can monas sp. is capable of promoting microalgal growth. It is believed accumulate lipids higher than this quantity, the production costs that the associated bacteria reduce photosynthetic oxygen tension offset by using wastewater must also be considered. In a related of phototrophic microalgae by consuming O2 as their electron study, untreated carpet industry wastewater was used for the cul- acceptor. It is also postulated that the algae-bacteria symbiosis is tivation of a microalgal consortium in polybags. The resultant bio- beneficial for algae as they can supply essential nutrients like vita- mass was rich in proteins (53.8%) with a biomethane generation mins and other compounds, as many algae are auxotrophic for À À potential of about 12,128 m3 biomethane ha 1 year 1 (Chinnasamy cobalamine (Croft et al., 2005). Siderophores present in some bac- et al., 2010a). The marine microalga Nannochloropsis gaditana was teria can promote microalgal growth under iron deficient condi- grown with centrate (i.e., concentrated municipal wastewater gen- tions (Amin et al., 2009). Also, the extracellular sheath erated during sludge centrifuge) as a sole nutrient source diluted in (composed of various sugars) present in some algae provide sites À À seawater (30–50%), with a biomass productivity of 0.4 g L 1 d 1 of attachment as well as organic carbon sources for bacterial and lipid accumulation of 20–25% DW. The biomass content was growth, and photosynthetic oxygen as electron acceptor for aero- similar to that obtained with nutrient media under laboratory con- bic respiration (Park et al., 2008). In a similar study, it was shown ditions, indication the richness of removable nutrients in centrate. that the associated bacteria plays a profound role in improving In addition, some macroalgae, such as Sargassum cymosum, have flocculation of Chlorella vulgaris, by increasing the floc size result- been used for biosorption or bio-accumulation of heavy metals ing in the sedimentation of microalgae (Lee et al., 2013). In the (such as Cu, Pb, and Ge) (Costa et al., 2016). Some brown- co-cultivation system, microalgae-bacteria consortium is usually macroalgae (e.g., Ascophyllum nodosum, Fucus spiralis, Laminaria formed by self-coagulation between algae and bacteria. Several hyperborea and Pelvetia canaliculata) can remove transition metal advantages can be observed in an algae-bacteria consortium sys- ions from petrochemical wastewaters (Cechinel et al., 2016). These tem: (1) The co-cultivation of algae and bacteria not only reduces observations can be used as a guideline to choose the microalgal high costs, but also decrease the spatial distance for O2 and CO2 strain for a particular purpose, as the choice of microalgae for exchange, when compared to separate culture units. (2) Starvation, wastewater treatment is based primarily on the pollutants the the main strategy used to trigger carbohydrate/lipid accumulation, microalgae need to deal with. In other words, for different wastew- can be achieved by manipulating the nutrient content in the med- ater sources, the mechanisms of microalgal wastewater treatment ium, similar to laboratory cultivation methods. (3) Enhanced bio- should be different. Fig. 3 illustrates the four main mechanisms mass harvesting efficiency (Xu et al., 2016) because of the auto- (i.e., bio-adsorption, bio-accumulation, bio-coagulation and bio- flocculation and co-flocculation properties of the constituent conversion) involved in microalgae-based wastewater treatment, microbiota. which will be critically discussed in the following sections. Y. Wang et al. / Bioresource Technology 222 (2016) 485–497 489

Texle dye wastewater

Heavy metal Biodegradaon

Dye compound Adsorpon precipitaon Bioadsorpon for + + + decolorizaiton

Accumulaon CO2

CO2 Redox enzyme

Bacteria EPS increasing CO2 Aerobic bacteria O Intermediates with low 2 toxicity

O2 Organic Anoxidave defense carbon mechanisms N source P source Agro-industrial wastewater Pharmaceucal wastewater

Fig. 3. Mechanisms of various industrial wastewater treatments using microalgae and bacteria.

Table 1 Symbiotic association between algae and bacteria in the algae-bacteria consortium.

Benefits Drawbacks

Algae  CO2 from bacterial metabolism  Algicidal effects of some bacteria  Stimulative effects and essential nutrients from bacterial metabolism  Enhanced flocculation by associated bacteria Bacteria  Oxygenation from algae  Increase in pH due to associated algal metabolism  Algal organic matter as a carbon source  Increase in temperature due to associated algal metabolism  Antibacterial effects from some algae

The formation of microalgae-bacteria consortium is dynamic input supports the production of 16.8 g of oxygen, which is suffi- and is usually divided into four stages. Stage 1: Adsorption of cient to oxidize another 5.6 g of nitrogen (Karya et al., 2013). microalgae onto the surface of flocculated sludge, probably due Therefore, the ideal nitrogen flux in the co-cultivation system is to extracellular polymeric substance (EPS) bridging and large that 15% of nitrogen is taken up by algae and 85% of them are superficial area of the activated sludge flocs (Salim et al., 2014). removed through the nitrification route, demonstrating that higher Stage 2: Attachment of the nascent bacteria onto the surface of percentage of nitrifying bacteria would face oxygen deficiency microalgae, mainly to the phycosphere on the surface of algal cell because the remaining algae would not be able to produce suffi- and its immediate environs (Eigemann et al., 2013). Stage 3: Uni- cient oxygen for full nitrification. Su et al. found that assimilation form distribution of microalgae and bacteria in the pellet, accom- of nitrogen into biomass can reach 61–93% of nitrogen removal panied by growth of both of the constituent biota (Su et al., in batch wastewater treatment reactors with co-culture of algae 2011). Stage 4: Formation of mature consortium (i.e., dynamic bal- and bacteria (Su et al., 2011). Karya et al. also found that 81–85% ance between biomass attachment and detachment), which is con- of the ammonium supplement was converted to NO3- by algae- sidered to be synergistic between algae and bacteria (Xu et al., bacteria consortium (Karya et al., 2013). Biological nitrification 2016). Algal exudates are the main carbon source for bacteria, has been shown to have the ability of solving certain problems, while algae can also benefit from bacteria as it provides CO2 and such as poor settling characteristics, during algal treatment of high nutrients through organic matter decomposition. Several studies ammonium-containing wastewaters (Su et al., 2011). A two-phase have combined microalgal photosynthesis with conventional photoperiod approach (consisting of a 12 h:60 h Light-Dark cycle, wastewater treatment. Indirect adhesion of bacterial symbionts followed by a 12 h:12 h Light-Dark cycle) was capable of efficient on the sheath and the direct adhesion onto the algal cell surface nutrient removal and enhanced biomass and lipid productivity may reduce diffusion distance and permit rapid and efficient by a well-balanced microbial consortia consisting of algae (Scene- exchange of substrates (Park et al., 2008). desmus) and bacteria (Flavobacteria, Sphingobacteria and Proteobac- In the algae-bacteria consortium system, algae produce oxygen teria (Lee et al., 2016). A similar approach of alternate light and for nitrification through photosynthesis, which reduces aeration dark photoperiod based cultivation was used for shortcut nitrogen demands. Removal of nitrogen can be achieved through assimila- removal using algae-bacterium consortia, where O2 production by tion by biomass and nitrification/denitrification with different photosynthetic activity stimulates ammonium-oxidizing-bacteria reaction mechanisms, which is dependent on the wastewater char- (AOB) during light period, and during the dark period, dissolved acteristics and reactor operating regime. Theoretically, 1 g of N oxygen (DO) is quickly consumed by microbial activity and algal 490 Y. Wang et al. / Bioresource Technology 222 (2016) 485–497

Table 2 Different microalgae-bacteria consortia used in wastewater treatment.

Microalgae-bacteria consortium Wastewater Pollutant removal Reference COD Nitrogen Phosphorus Note (%) (%) (%) Chlorella vulgaris + activated sludge Synthetic 83.6 89.4 91.4 Settling ability increased Xu et al. wastewater compared with pure microalgae (2016) Consortium of algae, consisting primarily of Chlorella Anaerobically NA NA 90 Photo-sequencing batch reactor Wang et al. (95.2%), Chlamydomonas (3.1%), and Stichococcus digested swine (PSBR); using organic carbon (2015a) (1.1%) + bacteria manure source Chlorella vulgaris + Azospirillum brasilense Synthetic NA 99 83 de-Bashan wastewater (2002) Chlorella sorokiniana + Azospirillum brasilense Municipal NA NA 72 Hernandez wastewater et al. (2006) Chlorella. sorokiniana + Azospirillum brasilense Ammonia NA 100 NA Higher temperatures (40 °C) and de-Bashan wastewater intensity of light et al. (2008) (2500 lmol mÀ2 sÀ1) Chlorella vulgaris + Lemna minuscula Recalcitrant 61 71.6 28 Ethanol and citric acid production Valderrama effluent et al. (2002) Scenedesmus sp. + Bacteria group Municipal 92.3 95.7 98.1 Bacteria: Flavobacteria and Lee et al. wastewater Sphingobacteria (2016) Chlorella. sorokiniana + aerobic sludge Swine 62.3 82.7 58.0 Nitrification efficiency: 75.7 % Hernandez wastewaters denitrification efficiency: 53.8% et al. (2013) Oscillatoria sp. OSC + Proteobacteria naturally associated Oil compounds in NA NA NA n-Octadecane 40% Abed and with Oscillatoria sp. wastewater pristine 50% Koster phenanthrene 50% (2005) dibenzothiophene 80% Cyanobacterial mats + Acinetobacter calcoaceticus and Oil compounds NA NA NA Oil 63.2% (0.5% v/v) Al-Awadhi Nocardioforms et al. (2003) Chlorella sorokiniana 211/8k + Ralstonia basilensis Toxic compounds NA Sodium salicylate removal Guieysse 1 mmol lÀ1 day et al. (2002) respiration to promote denitritation (Wang et al., 2015a). The total nutrients from wastewater (de-Bashan et al., 2004). Currently, energy influx into the photobioreactors comes from both organic many studies have investigated the co-culture of Chlorella sp. nutrients and light sources. with Azospirillum sp. in alginate beads, in order to treat wastewater Mass balance between microalgae and bacteria could be eluci- via the microalgae-bacteria consortium (de-Bashan, 2002) dated through a stable culture system (e.g., chemostat), while pho- (Table 2). tosynthetic activity (such as the CO2 assimilation rate by algae) Even though there are many reports regarding treatment of should be monitored in a precise and dynamic way (Lee et al., various wastewaters with microalgae-bacteria consortium, the 2016). In the microalgae-bacteria consortia, the bacterial propor- focus was mainly on the efficiency of nutrient removal, not bio- tion serves as the CO2 supplier to provide inorganic carbon for mass or lipid production. In view of this, a co-culture of Scenedes- algae growth, where nearly 300 bacteria units per algae unit were mus sp. and indigenous municipal wastewater bacteria for the proposed to ensure a stable CO2 supply. However, it would be treatment of pretreated municipal wastewater was carried out. strongly affected by the species, bioreactors, or growth condition. An alternative light and dark cycle was employed during cultiva- The three main algae-bacteria consortium currently in use are tion which improved biomass productivity and lipid content. The as follows: (1) algae plus wastewater, (2) algae plus activated biomass productivity and lipid productivity were 282.6 and sludge, (3) co-culture of algae and assigned bacteria (such as 71.4 mg LÀ1 dayÀ1, respectively (Yang et al., 2000). A similar co- nitrogen-fixing bacteria Azospirillum). Major bacteria that usually culture of Chlorella sorokiniana and aerobic bacteria on primarily exist in initial wastewater were identified as members of the fol- treated potato industry wastewater with alternate light and dark lowing genera Arcobacter, Clostridium, Desulfobulbus, Flavobac- cycle yielded a biomass productivity of 26 mg LÀ1 dayÀ1 with a terium, Acidovorax, Bacteroides, Propionivibrio, Dechloromonas, lipid content of 30% DW (Al-Awadhi et al., 2003). In addition, Flexibacter, Pseudomonas, Rhodobacter, Enhydrobacter, Sphingobac- compared with photoautotrophic culture, mixotrophic cultivation terium, Paludibacter, Smithella, Pedobacter, and Zoogloea . The abun- (e.g., algal-bacteria co-culture system) could achieve higher dance of Proteobacteria, Flavobacteria and Sphingobacteria in algal growth rates because of the production of beneficial photosyn- cultures has been previously reported (Sapp et al., 2007). Depend- thetic metabolites. For example, under mixotrophic conditions, ing on the algal species in the algae-bacteria consortia and the the carbohydrate productivity of Scenedesmus could be increased immediate environs during the various growth stages of algae, three fold than autotrophic cultivation, due to corresponding the associated bacterial community structure can be affected in a organic carbon addition and enhanced algal biomass productivity species-specific manner. Co-cultures of bacteria and algae have (Ji et al., 2015). Moreover, extracellular organic matters (EOM) been examined, including both bacteria-algae consortia in nature were frequently secreted by the algae-bacteria consortium. Star- and artificially induced symbioses. For natural symbiosis, com- vation has been confirmed to promote bacterial aggregation and monly occurring bacterial species of Brevundimonas and Sphin- EPS stimulation (Zhou et al., 2014). EPS stimulation increases gomonas has been reported (Tate et al., 2013). For artificially the settle ability of biomass and reduces process costs in biomass induced algae-bacteria consortium, the use of nitrogen-fixing bac- harvesting. The increased EOM may originate from reserve starch, terium Azospirillum has been studied (de-Bashan, 2002). De-bashan which could play a crucial role in the flocculation of biomass via et al. identified the stimulation of microalgal growth by associated its highly charged polymer structure (Mikulec et al., 2015). How- bacteria and coined the term ‘‘MGPB” – Microalgal growth promot- ever, more studies are needed to elucidate the mechanisms of ing bacteria. The preliminary study included co-immobilization of EOM secretion and the role of bacteria (promoting or limiting) Chlorella sp. and Azospirillum brazilein for efficient removal of in an algae-bacteria consortium. Y. Wang et al. / Bioresource Technology 222 (2016) 485–497 491

4. Biological treatments of different wastewaters using whereas under the same condition, only 30% inhibition was microalgal cultures observed for C. mexicana (Xiong et al., 2016). Moreover, C. mexicana and S. obliquus could achieve a maximum of 35% and 28% biodegra- 4.1. Pharmaceutical wastewater dation of CBZ, respectively (Xiong et al., 2016). It was also found that a mixture of pharmaceutical compounds (including CBZ) could Pharmaceutically active compounds (PhACs), mainly present in strongly decrease the activity of ATP synthase in Pseudokirchner- aquatic environments, are emerging as a severe risk for both wild- iella subcapitata (Xiong et al., 2016), suggesting that PhACs can life and humans (Kolpin et al., 2002). Because of the flourishing interfere with energy transduction in the mitochondria and chloro- pharmaceutical industry, unfortunately, many PhACs have been plast of algae (Vannini et al., 2011). Recently, Matamoros et al. systematically detected in wastewater over past decades (Ternes, (2016) reported that the microalgal consortium, containing Chlor- 1998). Till date, the occurrence of more than 200 different PhACs ella sp. and Scenedesmus sp. can successfully remove 20% of CBZ in water body has been reported. For instance, the antibiotic cipro- from urban and synthetic wastewater, as shown in Table 3. floxacin has been found in aquatic environments at a concentration The removal of pharmaceutical compounds from wastewater by of up to 6.5 mg LÀ1 (Petrie et al., 2015). Harmful concentrations of algae-bacteria consortium could be by means of bioaccumulation these compounds in higher trophic level organisms and long term or biodegradation. However, the elucidation of the actual mecha- effects via bio-magnification in food chains are evident because of nism and the role of bacteria in such processes needs to be further the extensive therapeutic use of pharmaceutical compounds (PCs) investigated. A study regarding CBZ removal by microalgae showed (Kelly et al., 2007). Among these, the most commonly seen drugs that some key enzymes (e.g., SOD, and CAT) of phototrophic are non-steroidal anti-inflammatory drugs (NSAIDs) ibuprofen microorganisms would protect against the reactive oxygen species and diclofenac, antibiotics (such as erythromycin, roxithromycin, (ROS) toxicity via regulation of anti-oxidative defense mechanisms ketoconazole, quinolones, fluoroquinolones), b-blockers (propra- (Xiong et al., 2016), which are commonly identified as the nolol), anti-depressants and antiepileptics (carbamazepine) biomarkers (Zhang et al., 2012)(Fig. 3). The superoxide dismutase (Petrie et al., 2015). (SOD) activity in C. mexicana was increased by 1.3-fold at low CBZ À Microalgae are the primary producers in aquatic food chains, concentrations (50 mg L 1) whereas the SOD activity at higher con- À and they are the key indicators for assessing water quality and centrations (200 mg L 1) was significantly decreased (Xiong et al., eco-toxicity of pollutants (Stevenson and Graham, 2014). Bioreme- 2016). In another related study, Zhang et al. (2012) found that À diation of contaminated waters by mixotrophic microalgae is a low CBZ concentration (0.5–10 mg L 1) could induce superoxide solar power-driven, ecologically comprehensive and sustainable dismutase (SOD) and catalase (CAT) activities in microalgal cells. reclamation strategy (Xiong et al., 2016). Carbamazepine (CBZ) is Freitas et al. (2015) also demonstrated that the SOD activity in one of the most investigated compounds in pharmaceutical indus- Scrobicularia plana and Diopatra neapolitana would increase at the À try based wastewater for bio-remediation by microalgae. Chlamy- extremely low CBZ concentration (<6 lgL 1), whereas the SOD domonas mexicana and Scenedesmus obliquus were evaluated for activity of both species decreased with an increase in CBZ concen- the toxicity, cellular stress and biodegradation stability of carba- trations. This is because the stress induced by CBZ would signifi- mazepine (CBZ) (Xiong et al., 2016). The growth of S. obliquus cantly enhance the generation of ROS in algal cells, resulting in was significantly inhibited (nearly 97%) at 200 mg CBZ LÀ1, membrane lipid peroxidation and functional damage (Xiong

Table 3 Microalgae used in the treatment of pharmaceutical wastewaters.

Species Compounds Biodegradation Note Reference Chlamydomonas mexicana Carbamazepine 35% 97% growth inhibition at 100 mg LÀ1 Xiong et al. (2016) Scenedesmus obliquus Carbamazepine 28% 30% growth inhibition at 100 mg LÀ1 Xiong et al. (2016) Chlamydomonas pitschmannii Carbamazepine NA 31.3% growth inhibition at 100 mg LÀ1 Xiong et al. (2016) Miractinium resseri Carbamazepine NA 43.5% growth inhibition at 100 mg LÀ1 Xiong et al. (2016) À1 Scenedesmus obliquus Carbamazepine NA EC50 was 54.60 mg L Zhang et al. (2012) À1 Chlorella pyrenoidosa Carbamazepine NA EC50 was 33.11 mg L Zhang et al. (2012) Scenedesmus quadricauda Pharmaceutical wastewater Absorption Microalgae can tolerance 20% PCTEa Vanerkar et al. (2015) Chlorella kessleri Pharmaceutical wastewater NA 13 psychoactive pharmaceuticals were selected Mackulak et al. for experiment (2015) Microalgae consortium Wastewater containing emerging Up to 90% 4-octylphenol, galaxolide, and tributyl Matamoros et al. contaminants phosphate concentrations (2016) Microalgae consortium Wastewater containing emerging 17% Caffeine Matamoros et al. contaminants (2016) Consortia of microalgae and bacteria Wastewater containing emerging 99% Caffeine Matamoros et al. in wastewater contaminants (2016) Microalgae consortium Wastewater containing emerging 15% Ibuprofen Matamoros et al. contaminants (2016) Consortia of microalgae and bacteria Wastewater containing emerging 60% Ibuprofen Matamoros et al. in wastewater contaminants (2016) Consortia of microalgae and bacteria Wastewater containing emerging <20% Carbamazepine and tris(2-chloroethyl) Matamoros et al. in wastewater contaminants phosphate (2016)

NA: not available. a PCTE: Physico-chemically treated effluent. 492 Y. Wang et al. / Bioresource Technology 222 (2016) 485–497

Table 4 Microalgae used for the treatment of textile dye from wastewaters.

Species Compounds Mechanism Note Reference Chlorella vulgaris Lanaset Red 2GA Adsorption 44% dye removal from initial concentration of 7.5 mg LÀ1 Chu et al. (2009) (immobilized in 2% alginate) Chlorella vulgaris Supranol Red 3BW Adsorption High rate algae ponds 50% color removal Zhou et al. (2014) Chlorella vulgaris mono-azo dye yellow 2G Bio- 63–90% color removal Acuner and Dilek sorption (2004) Chlorella vulgaris Remazol Black B, Remazol Red RR, Adsorption Aksu and Tezer Remazol Golden Yellow (2005) Chlorella sp. Indigo textile dye Adsorption 46% color removal Cheriaa et al. (2009) Caulerpa lentillifera Astrazon Blue FRGL Adsorption Dried algae biomass used as biosorbent Marungrueng and Pavasant (2006) Caulerpa lentillifera CI Basic Blue, CI Basic Red, CI Basic Adsorption Algae biomass can sequester Red GTLN more rapidly Marungrueng and Blue when compared with activated carbon Pavasant (2007) Synechocystis and reactive dye Bio- Cyanobacteria can be used for dye removal with Karacakaya et al. Phormidium adsorption stimulation of biomass production (2009) Phormidium. sp Remazol Blue and Reactive Black B Adsorption 88% color removal Ertugrul et al. (2008) Spirogyra Synazol Adsorption 85% decolorizaiton with dried biomass Khalaf (2008) Hypnea valentiae Dye Adsorption 88% decolorizaiton with dried biomass Khalaf (2008) Nostoc linckia Methyl red Degradation 82% color removal El-Sheekh et al. (2009) Lyngbya lagerlerimi Orange II Degradation 47% color removal El-Sheekh et al. (2009) Nostoc linckia Basic cationic Degradation 92% color removal El-Sheekh et al. (2009) Chlorella vulgaris G-Red (FN-3G) Degradation 59% color removal El-Sheekh et al. (2009) Oscillatoria rubescens Basic Fuschin Degradation 95% color removal El-Sheekh et al. (2009)

et al., 2016). In addition, the ROS formation caused by accumulated to azo dyes, and it can even grow in the presence of 400 mg LÀ1 CBZ could damage the cell structure and related physiological and of tectilon yellow 2G (a mono-azo dye) (Acuner and Dilek, 2004) biochemical processes (Dordio et al., 2011; Ke et al., 2010). It has (Table 4). In comparison, some algae species (e.g., Pseudokirchner- also been reported that the microalgal biodegradation prevented iella subcapitata, Selenastrum caprincornutum) are very sensitive À1 the formation of toxic intermediates (such as carcinogenic com- to azo dyes where their IC50 can be as low as 0.5 mg L pounds), which can be considered a significant achievement for (Novotny et al., 2006). C. vulgaris can remove 63–69% of color from the microalgal biodegradation (Xiong et al., 2016). Considering tectilon yellow 2G by converting it to aniline (Acuner and Dilek, the fact that thousands of PhACs and tons of PhACs containing 2004). The ability of C. vulgaris to break down the azo bond has also wastewater are generated every year, it is of urgent demand to find been observed by Lim et al. (2010) while treating textile wastewa- effective means to deal with this type of wastewater. A promising ter with the microalgal strain. Macroalgae, such as Caulerpa lentil- area for future research is to identify the role of algae-bacteria con- lifera (a green seaweed), can also remove basic dyes via biosorption sortium in degradation of PhACs, thereby providing a feasible way and the dye adsorption efficiency of this green seaweed was highly for efficient treatment of such wastewaters. correlated with the dye concentration in wastewater (Marungrueng and Pavasant, 2006). On the other hand, cyanobac- 4.2. Dye-containing wastewater teria, such as Synechocystis sp. and Phormidium sp., was also found to effectively remove reactive dye metabolically and the removal Textile industries commonly release a vast amount of wastew- efficiency was enhanced with the addition of specific plant growth ater, which contains various fabric dyes as the main constituent. regulator triacontanol hormone (Karacakaya et al., 2009). There are more than 100,000 commercially available dyes, and Previous studies showed that the mechanism of color removal more than 7 Â 105 tons of dyestuffs are produced worldwide by Chlorella sp. is mainly due to biosorption (Chu et al., 2009)as annually (Robinson et al., 2001). Textile industrial wastewater is shown in Fig. 3. To further understand the mechanism of microal- characterized by strong color, high salinity, high temperature, vari- gal biosorption, the related adsorption equilibriums were applied able pH and high chemical oxygen demand (COD). In general, most for evaluating the adsorption type. Freundlich, Langmuir, textile industries handle a huge quantity of synthetic dyes, sodium Redlich-Peterson and Koble-Corrigan adsorption models were sulphide, Glauber salt (in dye bath solution), and hydrogen perox- employed for the mathematical description of biosorption equilib- ide (as oxidizing agent) (Vijayaraghavan and Shanthakumar, 2015). rium, together with evaluating the isotherm constants at different Algae have been used to remove these colorful dyes through temperatures (Aksu and Tezer, 2005). Algae have been found to be biosorption or reductive mechanisms (Fig. 3). It was reported that potential bio-sorbents due to their rapid growth, relatively high more than 30 azo dyes could be decomposed by Chlorella sp. and surface area, and high binding affinity. Algal cell walls offer a host Oscillatoria sp. to aromatic amines that were further completely of functional groups including amino, carboxyl, sulphates, phos- metabolized by bacterial cultures (Jinqi and Houtian, 1992). phates, and imidazoles associated with polysaccharides, alginic Marungrueng and Pavasant (2007) also mentioned that the Cau- acid and proteins for binding various pollutants. The adsorption lerpa lentillifera can effectively remove three basic dyes (CI Basic of reactive dyes (e.g., Remazol Red and Remazol Golden Yellow) Blue, CI Basic Red, CI Basic Blue) by biosorption. by dried biomass of C. vulgaris followed the Langmuir model To use microalgal cells as the bio-sorbent or bio-coagulator, (Aksu and Tezer, 2005), suggesting that the dyes were adsorbed their growth tolerance to various dyes should be considered. For on monolayer coverage on homogenous sites of algal cell wall. instance, studies have shown that C. vulgaris has high tolerance On the other hand, conformation to Freundlich model suggests Y. Wang et al. / Bioresource Technology 222 (2016) 485–497 493 the existence of a heterogeneous surface with sorption sites of dif- produced by bacteria can bind significant concentrations of aque- ferent affinities. The possibility of the dyes being absorbed into the ous cations (e.g., Cd), which in turn influences the speciation, distri- cell and then transformed through bioconversion is worthwhile for bution and mobility of such cations in aqueous systems (Ueshima further investigation. et al., 2008). An algae-bacteria consortium comprising C. sorokini- Several studies have provided some exciting ideas for algae- ana and R. basilensis was found capable of metabolizing salicylate based dye wastewater treatment. First, extracellular polymeric with subsequent removal of heavy metals from solution (Munoz substances (known as EPS) and fluidity of the membrane could et al., 2006). It was also reported that copper cations could be contribute to the adsorption process. For instance, Enteromorpha removed more efficiently by an algae-bacteria consortium com- polysaccharide is one of the common fouling generated by green pared with individual constituent organism (Boivin et al., 2007), algae, which has caused serious environmental problems in past suggesting that metal removal by the consortium is a synergistic years. However, these Enteromorpha polysaccharides now are effect. serving as a new-type coagulant for color removal because of its Future research direction for algae-bacteria consortium based possible role as a bridging agent in floc formation (Zhao et al., heavy metal removal can involve the following points to be 2014). Second, the biofilm produced by algae-bacteria consortium addressed: (1) The mechanism of algae-bacteria consortium for system has high potential for dye wastewater treatment. A novel heavy metal removal, such as biosorption, bio-convention or bio- photobioelectrochemical system (PBES) was developed by accli- accumulation, should be systematically investigated, (2) The syn- mating algae-bacteria biofilm in anode and cathode, using C. vul- ergistic effects of algae and bacteria need more elucidation. (3) garis and indigenous wastewater bacteria, respectively, as the Ecological cation-exchanger can be developed, since dried biomass inoculum (Sun et al., 2015). The synergy between C. vulgaris and of algae and bacteria possess the ability of ion exchange due to mixed bacteria was responsible for the successful operation of charged cell walls. PBES, which can be potentially applied to treat wastewater con- taining azo dye, along with additional benefits of enhanced azo dye degradation, high net power output, and buffer minimization 4.4. Agro-industrial wastewater (Sun et al., 2015). Third, cyanobacteria have also been applied for dye pollutants removal because of its coagulation behavior and floc Agro-industrial wastewaters include potato processing wastew- characteristics (i.e. hydroxide flocs) (Karacakaya et al., 2009). ater, swine wastewater (Wang et al., 2015b), livestock wastewater, Finally, different algal species were compared for various dye dairy wastewater (Gentili, 2014), slaughterhouse wastewater, fish removal efficiencies to provide the detailed information on algae- farm wastewater and some digestion effluent. One common char- based dye wastewater treatments. In particular, the ability of C. acteristic of agro-industrial wastewater is high ammonium con- vulgaris, Lyngbya lagerlerimi, Nostoc lincki, Oscillatoria rubescens, centration, which is highly correlated to eutrophication (Wang Elkatothrix viridis and Volvox aureus to decolorize and remove et al., 2015b). Many microalgae can grow well under ‘‘nutrient- methyl red, orange II, G-Red (FN-3G), basic cationic, and basic rich” environment and rapidly convert the nutrients (e.g., ammo- fuchsin was investigated (El-Sheekh et al., 2009). The color nium used as a nitrogen source) contained in agro-industrial removal efficiency of these algae is dependent on different species, wastewaters to biomass (Wang et al., 2015b). The microalgae growth stage, cultivation conditions, as well as the molecular Neochloris oleoabundans, C. vulgaris and S. obliquus were cultivated structure of the dye. using agro-zootechnical digestate and compared for their ability in nitrogen removal and lipid production (Franchino et al., 2013). 4.3. Metal-containing wastewater However, some agro-industrial wastewaters are characteristic of high COD levels, (i.e., 20,180 mg LÀ1)(Wang et al., 2015b), and thus Many studies have clearly demonstrated the potential of metal it may not be easy to directly treat the original wastewaters by removal from wastewater by algal biomass. Cell walls of algae and microalgae. Thus, most studies on microalgae-based treatment of cyanobacteria are composed of carbohydrates and polysaccharides such wastewaters are conducted with appropriate dilution of orig- with negatively-charged groups (e.g. hydroxyl, amino, carboxyl or inal wastewater or employing anaerobic digestion as the pretreat- sulfhydryl group). Most positively-charged metals can tightly bind ment. Under optimal conditions, the ammonium removal to the negatively-charged ligand groups, which is the basis of efficiency by microalgae can often reach higher than 90% (Wang metal removal from metal containing wastewater (Fig. 3). In addi- et al., 2012, 2015b). Cyanobacteria are also very efficient in nitro- tion to adsorption onto cell surfaces, other mechanisms for effi- gen removal. Some cyanobacteria, such as Oscilatoria sp., Anabaena cient metal removal include bioaccumulation (uptake by cells or sp. and Spirulina sp., are capable of utilizing elemental nitrogen as incorporation into vacuoles), formation of chelates (such as arago- their sole nitrogen source, by the reduction of N2 to ammonium nite structures) and internal or surface precipitation. Thus, algae (Markou and Georgakakis, 2011). In general, the order in which À growing in wastewaters may provide a simple, long-term strategy cyanobacteria prefer to utilize nitrogen is ammonium > NO3 >N2. for removal of metal pollutants. Meanwhile, dried algal, cyanobac- The uptake of nitrate is mostly light dependent, and since the terial and bacterial biomass can also be applied for removal of reduction of nitrite consumes energy, cyanobacteria are inclined heavy metals from wastewaters (such as petrochemical to assimilate the reduced nitrogen (e.g., ammonium). Thus, co- wastewater) as cation exchanger, and metals can be recovered sub- culture of microalgae and cyanobacteria for ammonium-rich sequently by desorption with acids or other desorbing agents agro-industrial wastewater would be a potential solution. More- (Vijayaraghavan and Yun, 2008). Efficient removal of copper over, it has been reported that nitrate consumption in wastewater (80%) and cadmium (100%) from metal-containing wastewater will be reduced due to the high turbidity, which will increase treat- via a mixture of dried algal biomass was observed obtaining a max- ment costs. In addition, high concentrations of ammonium will imum removal rate within 5 min contact time (Loutseti et al., inhibit uptake of nitrate, because ammonium represses the synthe- 2009). However, it was also reported that heavy metals are potent sis of nitrate reductase, while high nitrate concentration inhibits inhibitors of photosynthesis because of their ability to replace or ammonia uptake. High temperatures favor the formation of free block the prosthetic metal atoms in the active sites of certain pho- ammonia. Although free ammonia is generally toxic to photosyn- tosynthesis related enzymes. On the contrary, the acidic functional thetic organisms, the toxicity appears to be reduced in alkalophilic groups on bacterial cell walls or extracellular polysaccharides species such as S. platensis (Belkin and Boussiba, 1991). 494 Y. Wang et al. / Bioresource Technology 222 (2016) 485–497

Table 5 Photobioreactors (PBR) used for wastewater treatment using microalgae-bacteria consortia.

PBR Type Strain Nitrogen removal Note Reference Tubular biofilm S. quadricauda + enriched culture 0.092 g/L/day 1 g of N input supports the production of Gonzalez et al. (2008) of nitrifiers 16.8 g of oxygen, which is sufficient to oxidise another 5.6 g of nitrogen Tubular biofilm Microalgae + bacteria Below 0.01 mg LÀ1 in Dominate microalgae: Chlorella, Oocystis Krustok et al. (2015) effluent and Scenedesmus. Dominate bacteria: Aulacoseira, Stephanodiscus, Diatoma, Cryptophyceae and Melosira Photo-sequencing batch reactor Chlorella + bacteria 90% Without aeration Wang et al. (2015a) (PSBR) Sequencing batch reactors (MaB- Consortium of NA Microalgal bacterial flocs; Four industrial Van Den Hende et al. floc SBRs) microalgae/cyanobacteria wastewater (2014) High rate algae ponds Microalgae-bacteria consortia 80% Slaughterhouse wastewater, working volume 75 L

5. Photobioreactor design for microalgae-based wastewater needed in order to assure biomass productivity and nutrient treatment removal. In most studies, the horizontal biofilm photobioreactors attained higher nutrient removal but lower algal biomass produc- Currently, most of the microalgal bioreactors can be categorized tion. Improvement of photobioreactor design can effectively pro- into open and closed systems with suspended or immobilized cell mote nutrient removal. Wu et al. (2011) proposed a hybrid cultures. Examples of photobioreactors used for wastewater treat- bioreactor which simultaneously supports heterotrophic and auto- ment with microalgae-bacteria consortium are summarized in trophic algal-bacteria consortium for high-loading nutrients Table 5. The open pond culture system is generally regarded as removal, with 81% total phosphorus and 86% ammonium removal the most economical process among algae cultivation systems efficiency. In addition, common wastewater treatment reactor because of low operating costs and simple operation. However, (e.g., sequencing batch reactor, PBR) can be used for algae cultiva- open pound systems depend a lot on the natural environment of tion as well (Van Den Hende et al., 2014). The effective alternate pond site, and contamination is liable to happen. Types of open light-dark cultivation of microalgae-bacteria consortium in a pond system that are currently in use include slope system, race- photo-sequencing batch reactor (PSBR) can accomplish efficient way ponds and circular ponds and these have been developed for N and P removal without aeration (Wang et al., 2015a). Some decades. Hernández et al. used a high rate algal pond (HRAP) for biofilm-based wastewater treatment tank can also be used for treatment of slaughterhouse wastewater and showed >70% microalgae wastewater treatment, such as algae membrane biore- removal of ammonium under all experimental conditions by an actor (A-MBR). Xu et al. used an A-MBR to cultivate Chlorella vul- algae-bacteria consortium. In addition, oxidation of both organic garis in continuous mode, obtaining the highest total N (TN) matter and ammonium was achieved by the C. sorokiniana-mixed removal efficiency of 73.4 ± 6.3% and total P (TP) removal efficiency bacterial culture from the activated sludge process in the tubular of 91.3 ± 3.8% at a solid retention time (SRT) of 10 d and a HRT of biofilm photobioreactor (Gonzalez et al., 2008). 24 h (Xu et al., 2015). It was found that a shorter SRT seemed to Using closed photobioreactors for microalgal cultivation usually favor biomass production, while a longer SRT led to poorer cell require higher capital and operating costs but they are in general growth. According to Xu et al.’s study, the highest algal productiv- À À more efficient in cell growth due to better control of the culture ity (131.7 g m 3/d or 22.4 g m 2/d) was observed at the a short SRT conditions and lower contamination risks. Biomass production of 5 d (Xu et al., 2015). In addition, the operation of a microalgal and nutrient removal efficiencies can be improved by efficient cul- biofilm photobioreactor would be helpful for increasing nutrient ture techniques. In recent years, there are increasing interests in removal efficiency. Fernadez et al. developed a hierarchical control utilizing immobilized cultures (in particular, biofilm reactors) for strategy for microalgal production in a tubular photobioreactor, microalgae cultivation to obtain better performance during which efficiently reduced the algal cultivation cost to around microalgae-based wastewater treatment in contrast to conven- 100 €/kg and also lowered the CO2 loss to 167 g/d (Fernández tional suspended cultures. Biofilm based culturing is the common et al., 2016). immobilized culture system, which is promising for increasing In some microalgae-bacteria consortium biofilm reactors, the algal culture density with less water source and land space mechanical aeration can be replaced by photosynthetic aeration (Robinson et al., 2001). It has obvious advantages for biomass and EPS can serve as flocs (Van Den Hende et al., 2014). The stabil- and lipid/carbohydrate production, nutrient removal and lower ity of the flocculated microalgal-bacterial biomass was signifi- energy cost compared with suspended culture photobioreactors cantly affected by extracellular polymer substances (EPS). (e.g., tubular photobioreactor, plate photobioreactor). Christenson Moreover, the bacterial exopolymer can improve aggregation pos- and Sims (Christenson and Sims, 2012) compared the treatment sibilities of algae-bacteria consortium for increasing sedimentation of secondary effluent of municipal wastewater by rotating algae efficiency of the biomass. It can also be used as stabilizers for floc biofilm reactor (RABR), with the highest biomass productivity of formation. 31 g mÀ2 dÀ1, which is much higher than suspended system (bio- In previous Using carrier materials to immobilize the mass productivity of 7.4 g mÀ2 dÀ1). The EOM secreted by microal- microalgal-bacterial culture is another method for improving gae consists of polysaccharides, proteins, nucleic acids, and nutrient removal. However, the price of such carrier materials phospholipids, which contribute to biofilm formation as well must be very low to minimize the cost associated with wastewater (Wingender et al., 2012). treatment. The carrier materials should also be non-toxic (environ- Typical microalgal biofilm reactors employed in wastewater mentally friendly), structurally stable, promote enhanced mass treatment are limited to horizontal biofilm reactor and rotating transfer efficiency and economic. Munoz et al. (2009) used a bio- algal biofilm reactor (RABR). The horizontal biofilm reactor can film photobioreactor for C. sorokiniana-R. basilensis consortium receive light energy effectively, however, a large surface area is immobilized onto foamed-glass beads carrier and onto reactor wall Y. Wang et al. / Bioresource Technology 222 (2016) 485–497 495 for treating salicylate contaminant in wastewater. In addition, Christenson, L.B., Sims, R.C., 2012. Rotating algal biofilm reactor and spool harvester algae immobilized with active sludge for simultaneous COD and for wastewater treatment with biofuels by-products. Biotechnol. Bioeng. 109 (7), 1674–1684. nutrients removal has attracted more attention recently. In addi- Chu, W.L., See, Y.C., Phang, S.M., 2009. Use of immobilised Chlorella vulgaris for the tion to better waste reduction performance with the removal of colour from textile dyes. J. Appl. Phycol. 21 (6), 641–648. immobilized-cell system, it may also be easier and less expensive Costa, G.B., de Felix, M.R., Simioni, C., Ramlov, F., Oliveira, E.R., Pereira, D.T., Maraschin, M., Chow, F., Horta, P.A., Lalau, C.M., da Costa, C.H., Matias, W.G., to collector harvest the microalgal cells from biofilms for further Bouzon, Z.L., Schmidt, E.C., 2016. Effects of copper and lead exposure on the uses, making it an extra benefit by using the immobilized-cell cul- ecophysiology of the brown seaweed Sargassum cymosum. Protoplasma 253 (1), ture. Considering the lack of information regarding immobilized 111–125. Croft, M.T., Lawrence, A.D., Raux-Deery, E., Warren, M.J., Smith, A.G., 2005. Algae algae-bacteria systems, more carriers/supports should be exam- acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438 ined for the immobilization of algae-bacteria consortium in future (7064), 90–93. studies. Daneshvar, N., Ayazloo, M., Khataee, A.R., Pourhassan, M., 2007. Biological decolorization of dye solution containing Malachite Green by microalgae Cosmarium sp. Bioresour. Technol. 98 (6), 1176–1182. 6. Conclusions de-Bashan, L., 2002. Removal of ammonium and phosphorus ions from synthetic wastewater by the microalgae Chlorella vulgaris coimmobilized in alginate beads with the microalgae growth-promoting bacterium Azospirillum Microalgae and microalgae-bacteria consortium can be success- brasilense. Water Res. 36 (12), 2941–2948. fully applied for the treatment of nutrients-rich wastewater, such de-Bashan, L.E., Hernandez, J.P., Morey, T., Bashan, Y., 2004. Microalgae growth- promoting bacteria as ‘‘helpers” for microalgae: a novel approach for removing as agro-industrial wastewater, municipal wastewater, pharmaceu- ammonium and phosphorus from municipal wastewater. Water Res. 38 (2), tical wastewater and textile dye wastewaters by biosorption or 466–474. bio-conversion pathways. Several advantages are clearly observed de-Bashan, L.E., Trejo, A., Huss, V.A., Hernandez, J.P., Bashan, Y., 2008. Chlorella sorokiniana UTEX 2805, a heat and intense, sunlight-tolerant microalga with in an algae-bacteria consortium system. The resulting microalgal potential for removing ammonium from wastewater. Bioresour. Technol. 99 biomass obtained from wastewater treatment can be used for bio- (11), 4980–4989. fuels production or other applications to gain additional benefits, Di Caprio, F., Altimari, P., Pagnanelli, F., 2015. Integrated biomass production and biodegradation of olive mill wastewater by cultivation of Scenedesmus sp. Algal making it a feasible and reliable process for dual purposes of waste Res. 9, 306–311. reduction and biofuels generation. Nevertheless, some mecha- Dordio, A.V., Belo, M., Teixeira, D.M., Carvalho, A.J.P., Dias, C.M.B., Pico, Y., Pinto, A.P., nisms involved in pollutant removal and bio-conversion in 2011. Evaluation of carbamazepine uptake and metabolization by Typha spp., a plant with potential use in phytotreatment. Bioresour. Technol. 102 (17), 7827– microalgae-based wastewater treatment are still not clearly under- 7834. stood and require further investigations. Eigemann, F., Hilt, S., Salka, I., Grossart, H.P., 2013. Bacterial community composition associated with freshwater algae: species specificity vs. dependency on environmental conditions and source community. FEMS Acknowledgements Microbiol. Ecol. 83 (3), 650–663. El-Sheekh, M.M., Gharieb, M.M., Abou-El-Souod, G.W., 2009. Biodegradation of dyes by some green algae and cyanobacteria. Int. Biodeterior. Biodegradation 63 (6), This work was supported by Open Project of State Key Labora- 699–704. tory of Urban Water Resource and Environment, Harbin Institute of Ertugrul, S., Bakir, M., Donmez, G., 2008. Treatment of dye-rich wastewater by an Technology (HCK201607). The authors also gratefully acknowledge immobilized thermophilic cyanobacterial strain: Phormidium sp. Ecol. Eng. 32 the support received from Taiwan’s Ministry of Science and Tech- (3), 244–248. Fernández, I., Berenguel, M., Guzmán, J.L., Acién, F.G., de Andrade, G.A., Pagano, D.J., nology (MOST) under grant numbers 105-3113-E-006-003, 104- 2016. Hierarchical control for microalgae biomass production in 2221-E-006-227-MY3, and 103-2221-E-006-190-MY3. photobiorreactors. Control Eng. Pract. 54, 246–255. Franchino, M., Comino, E., Bona, F., Riggio, V.A., 2013. Growth of three microalgae strains and nutrient removal from an agro-zootechnical digestate. References Chemosphere 92 (6), 738–744. Freitas, R., Almeida, A., Calisto, V., Velez, C., Moreira, A., Schneider, R.J., Esteves, V.I., Wrona, F.J., Soares, A.M.V.M., Figueira, E., 2015. How life history influences the Abed, R.M.M., Koster, J., 2005. The direct role of aerobic heterotrophic bacteria responses of the clam Scrobicularia plana to the combined impacts of associated with cyanobacteria in the degradation of oil compounds. Int. carbamazepine and pH decrease. Environ. Pollut. 202, 205–214. Biodeterior. Biodegradation 55 (1), 29–37. Gentili, F.G., 2014. Microalgal biomass and lipid production in mixed municipal, Acuner, E., Dilek, F.B., 2004. Treatment of tectilon yellow 2G by Chlorella vulgaris. dairy, pulp and paper wastewater together with added flue gases. Bioresour. Process Biochem. 39 (5), 623–631. Technol. 169, 27–32. Aksu, Z., Tezer, S., 2005. Biosorption of reactive dyes on the green alga Chlorella Gonzalez, C., Marciniak, J., Villaverde, S., Leon, C., Garcia, P.A., Munoz, R., 2008. vulgaris. Process Biochem. 40 (3–4), 1347–1361. Efficient nutrient removal from swine manure in a tubular biofilm photo- Al-Awadhi, H., Al-Hasan, R.H., Sorkhoh, N.A., Salamah, S., Radwan, S.S., 2003. bioreactor using algae-bacteria consortia. Water Sci. Technol. 58 (1), 95–102. Establishing oil-degrading biofilms on gravel particles and glass plates. Int. Guieysse, B., Borde, X., Munoz, R., Hatti-Kaul, R., Nugier-Chauvin, C., Patin, H., Biodeterior. Biodegradation 51 (3), 181–185. Mattiasson, B., 2002. Influence of the initial composition of algal-bacterial Amin, S.A., Green, D.H., Hart, M.C., Kupper, F.C., Sunda, W.G., Carrano, C.J., 2009. microcosms on the degradation of salicylate in a fed-batch culture. Biotechnol. Photolysis of iron-siderophore chelates promotes bacterial-algal mutualism. Lett. 24 (7), 531–538. Proc. Natl. Acad. Sci. U.S.A. 106 (40), 17071–17076. He, P.J., Mao, B., Shen, C.M., Shao, L.M., Lee, D.J., Chang, J.S., 2013. Cultivation of Belkin, S., Boussiba, S., 1991. Resistance of spirulina-platensis to ammonia at high Chlorella vulgaris on wastewater containing high levels of ammonia for Ph values. Plant Cell Physiol. 32 (7), 953–958. biodiesel production. Bioresour. Technol. 129, 177–181. Boelee, N.C., Temmink, H., Janssen, M., Buisman, C.J., Wijffels, R.H., 2011. Nitrogen Hernandez, J.P., de-Bashan, L.E., Bashan, Y., 2006. Starvation enhances phosphorus and phosphorus removal from municipal wastewater effluent using microalgal removal from wastewater by the microalga Chlorella spp. co-immobilized with biofilms. Water Res. 45 (18), 5925–5933. Azospirillum brasilense. Enzyme Microb. Technol. 38 (1-2), 190–198. Boivin, M.E., Greve, G.D., Garcia-Meza, J.V., Massieux, B., Sprenger, W., Kraak, M.H., Hernandez, D., Riano, B., Coca, M., Garcia-Gonzalez, M.C., 2013. Treatment of agro- Breure, A.M., Rutgers, M., Admiraal, W., 2007. Algal-bacterial interactions in industrial wastewater using microalgae-bacteria consortium combined with metal contaminated floodplain sediments. Environ. Pollut. 145 (3), 884–894. anaerobic digestion of the produced biomass. Bioresour. Technol. 135, 598–603. Cechinel, M.A.P., Mayer, D.A., Pozdniakova, T.A., Mazur, L.P., Boaventura, R.A.R., de Ji, F., Liu, Y., Hao, R., Li, G., Zhou, Y., Dong, R., 2014. Biomass production and nutrients Souza, A.A.U., de Souza, S.M.A.G.U., Vilar, V.J.P., 2016. Removal of metal ions removal by a new microalgae strain Desmodesmus sp. in anaerobic digestion from a petrochemical wastewater using brown macro-algae as natural cation- wastewater. Bioresour. Technol. 161, 200–207. exchangers. Chem. Eng. J. 286, 1–15. Ji, M.K., Yun, H.S., Park, Y.T., Kabra, A.N., Oh, I.H., Choi, J., 2015. Mixotrophic Cheriaa, J., Bettaieb, F., Denden, I., Bakhrouf, A., 2009. Characterization of new algae cultivation of a microalga Scenedesmus obliquus in municipal wastewater isolated from textile wastewater plant. J. Food Agric. Environ. 7 (3–4), 700–704. supplemented with food wastewater and flue gas CO for biomass production. J. Chinnasamy, S., Bhatnagar, A., Hunt, R.W., Das, K.C., 2010a. Microalgae cultivation in 2 Environ. Manage. 159, 115–120. a wastewater dominated by carpet mill effluents for biofuel applications. Jinqi, L., Houtian, L., 1992. Degradation of azo dyes by algae. Environ. Pollut. 75 (3), Bioresour. Technol. 101, 3097–3105. 273–278. Chinnasamy, S., Bhatnagar, A., Claxton, R., Das, K.C., 2010b. Biomass and bioenergy Karacakaya, P., Kilic, N.K., Duygu, E., Donmez, G., 2009. Stimulation of reactive dye production potential of microalgae consortium in open and closed bioreactors removal by cyanobacteria in media containing triacontanol hormone. J. Hazard. using untreated carpet industry effluent as growth medium. Bioresour. Technol. Mater. 172 (2–3), 1635–1639. 101 (17), 6751–6760. 496 Y. Wang et al. / Bioresource Technology 222 (2016) 485–497

Karya, N.G., van der Steen, N.P., Lens, P.N., 2013. Photo-oxygenation to support Ruiz-Martinez, A., Serralta, J., Seco, A., Ferrer, J., 2015. Effect of temperature on nitrification in an algal-bacterial consortium treating artificial wastewater. ammonium removal in Scenedesmus sp. Bioresour. Technol. 191, 346–349. Bioresour. Technol. 134, 244–250. Salim, S., Kosterink, N.R., Tchetkoua Wacka, N.D., Vermue, M.H., Wijffels, R.H., 2014. Ke, L., Luo, L.J., Wang, P., Luan, T.G., Tam, N.F.Y., 2010. Effects of metals on Mechanism behind autoflocculation of unicellular green microalgae Ettlia biosorption and biodegradation of mixed polycyclic aromatic hydrocarbons by a texensis. J. Biotechnol. 174, 34–38. freshwater green alga Selenastrum capricornutum. Bioresour. Technol. 101 (18), Sapp, M., Schwaderer, A.S., Wiltshire, K.H., Hoppe, H.G., Gerdts, G., Wichels, A., 2007. 6950–6961. Species-specific bacterial communities in the phycosphere of microalgae? Kelly, B.C., Ikonomou, M.G., Blair, J.D., Morin, A.E., Gobas, F.A., 2007. Food web- Microb. Ecol. 53 (4), 683–699. specific biomagnification of persistent organic pollutants. Science 317 (5835), Stevenson, J., Graham, L., 2014. Ecological assessments with algae: a review and 236–239. synthesis. J. Phycol. 50 (3), 437–461. Khalaf, M.A., 2008. Biosorption of reactive dye from textile wastewater by non- Su, Y., Mennerich, A., Urban, B., 2011. Municipal wastewater treatment and biomass viable biomass of Aspergillus niger and Spirogyra sp. Bioresour. Technol. 99 accumulation with a wastewater-born and settleable algal-bacterial culture. (14), 6631–6634. Water Res. 45 (11), 3351–3358. Kim, H.C., Choi, W.J., Chae, A.N., Park, J., Kim, H.J., Song, K.G., 2016. Evaluating Sun, J., Hu, Y.Y., Li, W.J., Zhang, Y.P., Chen, J., Deng, F., 2015. Sequential integrated strategies for robust treatment of high saline piggery wastewater. decolorization of azo dye and mineralization of decolorization liquid coupled Water Res. 89, 222–231. with bioelectricity generation using a pH self-neutralized Kolpin, D.W., Furlong, E.T., Meyer, M.T., Thurman, E.M., Zaugg, S.D., Barber, L.B., photobioelectrochemical system operated with polarity reversion. J. Hazard. Buxton, H.T., 2002. Pharmaceuticals, hormones, and other organic wastewater Mater. 289, 108–117. contaminants in US streams, 1999–2000: a national reconnaissance. Environ. Talbot, P., Thébault, J.-M., Dauta, A., De la Noüe, J., 1991. A comparative study and Sci. Technol. 36 (6), 1202–1211. mathematical modeling of temperature, light and growth of three microalgae Krustok, I., Odlare, M., Shabiimam, M.A., Truu, J., Truu, M., Ligi, T., Nehrenheim, E., potentially useful for wastewater treatment. Water Res. 25 (4), 465–472. 2015. Characterization of algal and microbial community growth in a Tanabe, Y., Kato, S., Matsuura, H., Watanabe, M.M., 2012. A botryococcus strain with wastewater treating batch photo-bioreactor inoculated with lake water. Algal bacterial ectosymbionts grows fast and produces high amount of hydrocarbons. Res. Biomass Biofuels Bioprod. 11, 421–427. Procedia Environ. Sci. 15, 22–26. Lee, J., Cho, D.H., Ramanan, R., Kim, B.H., Oh, H.M., Kim, H.S., 2013. Microalgae- Tate, J.J., Gutierrez-Wing, M.T., Rusch, K.A., Benton, M.G., 2013. The effects of plant associated bacteria play a key role in the flocculation of Chlorella vulgaris. growth substances and mixed cultures on growth and metabolite production of Bioresour. Technol. 131, 195–201. green algae Chlorella sp.: a review. J. Plant Growth Regul. 32 (2), 417–428. Lee, C.S., Oh, H.S., Oh, H.M., Kim, H.S., Ahn, C.Y., 2016. Two-phase photoperiodic Ternes, T.A., 1998. Occurrence of drugs in German sewage treatment plants and cultivation of algal-bacterial consortia for high biomass production and efficient rivers. Water Res. 32 (11), 3245–3260. nutrient removal from municipal wastewater. Bioresour. Technol. 200, 867– Ueshima, M., Ginn, B.R., Haack, E.A., Szymailowski, J.E.S., Fein, F.B., 2008. Cd 875. adsorption onto Pseudomonas putida in the presence and absence of Lim, S.L., Chu, W.L., Phang, S.M., 2010. Use of Chlorella vulgaris for bioremediation extracellular polymeric substances. Geochim. Cosmochim. Acta 72 (24), of textile wastewater. Bioresour. Technol. 101 (19), 7314–7322. 5885–5895. Loutseti, S., Danielidis, D.B., Economou-Amilli, A., Katsaros, C., Santas, R., Santas, P., Valderrama, L.T., Del Campo, C.M., Rodriguez, C.M., de- Bashan, L.E., Bashan, Y., 2009. The application of a micro-algal/bacterial biofilter for the detoxification of 2002. Treatment of recalcitrant wastewater from ethanol and citric acid copper and cadmium metal wastes. Bioresour. Technol. 100 (7), 2099–2105. production using the microalga Chlorella vulgaris and the macrophyte Lemna Mackulak, T., Mosny, M., Grabic, R., Golovko, O., Koba, O., Birosova, L., 2015. Fenton- minuscula. Water Res. 36 (17), 4185–4192. like reaction: a possible way to efficiently remove illicit drugs and Van Den Hende, S., Carre, E., Cocaud, E., Beelen, V., Boon, N., Vervaeren, H., 2014. pharmaceuticals from wastewater. Environ. Toxicol. Pharmacol. 39 (2), 483–488. Treatment of industrial wastewaters by microalgal bacterial flocs in sequencing Markou, G., Georgakakis, D., 2011. Cultivation of filamentous cyanobacteria (blue- batch reactors. Bioresour. Technol. 161, 245–254. green algae) in agro-industrial wastes and wastewaters: a review. Appl. Energy Vanerkar, A.P., Fulke, A.B., Lokhande, S.K., Giripunje, M.D., Satyanarayan, S., 2015. 88 (10), 3389–3401. Recycling and treatment of herbal pharmaceutical wastewater using Martinez, M.E., Sanchez, S., Jimenez, J.M., El Yousfi, F., Munoz, L., 2000. Nitrogen and Scenedesmus quadricauda. Curr. Sci. 108 (5), 979–983. phosphorus removal from urban wastewater by the microalga Scenedesmus Vannini, C., Domingo, G., Marsoni, M., De Mattia, F., Labra, M., Castiglioni, S., Bracale, obliquus. Bioresour. Technol. 73 (3), 263–272. M., 2011. Effects of a complex mixture of therapeutic drugs on unicellular algae Marungrueng, K., Pavasant, P., 2006. Removal of basic dye (Astrazon Blue FGRL) Pseudokirchneriella subcapitata. Aquat. Toxicol. 101 (2), 459–465. using macroalga Caulerpa lentillifera. J. Environ. Manage. 78 (3), 268–274. Vijayaraghavan, G., Shanthakumar, S., 2015. Removal of sulphur black dye from its Marungrueng, K., Pavasant, P., 2007. High performance biosorbent (Caulerpa aqueous solution using alginate from sargassum sp (brown algae) as a lentillifera) for basic dye removal. Bioresour. Technol. 98 (8), 1567–1572. coagulant. Environ. Prog. Sustainable Energy 34 (5), 1427–1434. Matamoros, V., Uggetti, E., Garcia, J., Bayona, J.M., 2016. Assessment of the Vijayaraghavan, K., Yun, Y.S., 2008. Bacterial biosorbents and biosorption. mechanisms involved in the removal of emerging contaminants by Biotechnol. Adv. 26 (3), 266–291. microalgae from wastewater: a laboratory scale study. J. Hazard. Mater. 301, Wang, B., Lan, C.Q., 2011. Biomass production and nitrogen and phosphorus 197–205. removal by the green alga Neochloris oleoabundans in simulated wastewater and McGinn, P.J., Dickinson, K.E., Park, K.C., Whitney, C.G., MacQuarrie, S.P., Black, F.J., secondary municipal wastewater effluent. Bioresour. Technol. 102 (10), 5639– Frigon, J.-C., Guiot, S.R., O’Leary, S.J.B., 2012. Assessment of the bioenergy and 5644. bioremediation potentials of the microalga Scenedesmus sp. AMDD cultivated Wang, H., Xiong, H., Hui, Z., Zeng, X., 2012. Mixotrophic cultivation of Chlorella in municipal wastewater effluent in batch and continuous mode. Algal Res. 1 pyrenoidosa with diluted primary piggery wastewater to produce lipids. (2), 155–165. Bioresour. Technol. 104, 215–220. Mikulec, J., Polakovicova, G., Cvengros, J., 2015. Flocculation using polyacrylamide Wang, M., Yang, H., Ergas, S.J., van der Steen, P., 2015a. A novel shortcut nitrogen polymers for fresh microalgae. Chem. Eng. Technol. 38 (4), 595–601. removal process using an algal-bacterial consortium in a photo-sequencing Munoz, R., Alvarez, M.T., Munoz, A., Terrazas, E., Guieysse, B., Mattiasson, B., 2006. batch reactor (PSBR). Water Res. 87, 38–48. Sequential removal of heavy metals ions and organic pollutants using an algal- Wang, Y., Guo, W., Yen, H.W., Ho, S.H., Lo, Y.C., Cheng, C.L., Ren, N., Chang, J.S., bacterial consortium. Chemosphere 63 (6), 903–911. 2015b. Cultivation of Chlorella vulgaris JSC-6 with swine wastewater for Munoz, R., Kollner, C., Guieysse, B., 2009. Biofilm photobioreactors for the treatment simultaneous nutrient/COD removal and carbohydrate production. Bioresour. of industrial wastewaters. J. Hazard. Mater. 161 (1), 29–34. Technol. 198, 619–625. Novotny, C., Dias, N., Kapanen, A., Malachova, K., Vandrovcova, M., Itavaara, M., Wilkie, A.C., Mulbry, W.W., 2002. Recovery of dairy manure nutrients by benthic Lima, N., 2006. Comparative use of bacterial, algal and protozoan tests to study freshwater algae. Bioresour. Technol. 84 (1), 81–91. toxicity of azo- and anthraquinone dyes. Chemosphere 63 (9), 1436–1442. Wingender, J., Neu, T.R., Flemming, H.-C., 2012. Microbial Extracellular Polymeric Park, Y., Je, K.W., Lee, K., Jung, S.E., Choi, T.J., 2008. Growth promotion of Chlorella Substances: Characterization, Structure and Function. Springer Science & ellipsoidea by co-inoculation with Brevundimonas sp isolated from the Business Media. microalga. Hydrobiologia 598, 219–228. Wu, Y., Hu, Z., Yang, L., Graham, B., Kerr, P.G., 2011. The removal of nutrients from Petrie, B., Barden, R., Kasprzyk-Hordern, B., 2015. A review on emerging non-point source wastewater by a hybrid bioreactor. Bioresour. Technol. 102 contaminants in wastewaters and the environment: current knowledge, (3), 2419–2426. understudied areas and recommendations for future monitoring. Water Res. Xiong, J.Q., Kurade, M.B., Abou-Shanab, R.A.I., Ji, M.K., Choi, J., Kim, J.O., Jeon, B.H., 72, 3–27. 2016. Biodegradation of carbamazepine using freshwater microalgae Polishchuk, A., Valev, D., Tarvainen, M., Mishra, S., Kinnunen, V., Antal, T., Yang, B., Chlamydomonas mexicana and Scenedesmus obliquus and the determination of Rintala, J., Tyystjarvi, E., 2015. Cultivation of Nannochloropsis for its metabolic fate. Bioresour. Technol. 205, 183–190. eicosapentaenoic acid production in wastewaters of pulp and paper industry. Xu, M., Li, P., Tang, T., Hu, Z., 2015. Roles of SRT and HRT of an algal membrane Bioresour. Technol. 193, 469–476. bioreactor system with a tanks-in-series configuration for secondary Prandini, J.M., da Silva, M.L., Mezzari, M.P., Pirolli, M., Michelon, W., Soares, H.M., wastewater effluent polishing. Ecol. Eng. 85, 257–264. 2016. Enhancement of nutrient removal from swine wastewater digestate Xu, Y.J., Wang, Y., Yang, Y., Zhou, D.D., 2016. The role of starvation in biomass coupled to biogas purification by microalgae Scenedesmus spp. Bioresour. harvesting and lipid accumulation: Co-culture of microalgae-bacteria in Technol. 202, 67–75. synthetic wastewater. Environ. Prog. Sustainable Energy 35 (1), 103–109. Robinson, T., McMullan, G., Marchant, R., Nigam, P., 2001. Remediation of dyes in Yang, C., Hua, Q., Shimizu, K., 2000. Energetics and carbon metabolism during textile effluent: a critical review on current treatment technologies with a growth of microalgal cells under photoautotrophic, mixotrophic and cyclic proposed alternative. Bioresour. Technol. 77 (3), 247–255. light-autotrophic/dark-heterotrophic conditions. Biochem. Eng. J. 6 (2), 87–102. Y. Wang et al. / Bioresource Technology 222 (2016) 485–497 497

Zhang, W., Zhang, M., Lin, K., Sun, W., Xiong, B., Guo, M., Cui, X., Fu, R., 2012. Eco- Zhou, D., Niu, S., Xiong, Y., Yang, Y., Dong, S., 2014. Microbial selection pressure is toxicological effect of carbamazepine on Scenedesmus obliquus and Chlorella not a prerequisite for granulation: dynamic granulation and microbial pyrenoidosa. Environ. Toxicol. Pharmacol. 33 (2), 344–352. community study in a complete mixing bioreactor. Bioresour. Technol. 161, Zhao, S., Gao, B.Y., Yue, Q.Y., Wang, Y., Li, Q., Dong, H.Y., Yan, H., 2014. Study of 102–108. Enteromorpha polysaccharides as a new-style coagulant aid in dye wastewater treatment. Carbohydr. Polym. 103, 179–186. Zhou, W., Li, Y., Min, M., Hu, B., Chen, P., Ruan, R., 2011. Local bioprospecting for high-lipid producing microalgal strains to be grown on concentrated municipal wastewater for biofuel production. Bioresour. Technol. 102 (13), 6909–6919.