Algal culture and biofuel production using wastewater

CHAPTER

Algal culture and biofuel production using wastewater

8

Shih-Hsin Ho⁎, Yi-Di Chen⁎, Wen-Ying Qu⁎, Fei-Yu Liu⁎, Yue Wang†, State Key Laboratory of Urban Water Resource and Environment, School of Municipal and Environmental Engineering, Harbin Institute of Technology, Harbin, People’s Republic of China⁎ College of Life Sciences and Oceanography, Shenzhen University, Shenzhen, People’s Republic of China†

1 ­INTRODUCTION With the increasing development of society and the growth rate of the population, environmental issues become increasingly severe. Wastewaters contain significant organic load, total nitrogen (TN), total phosphorus (TP), heavy metals (HMs), and chemicals. Therefore, a large volume of wastewater must be treated to prevent environmental pollution, and to protect public health by ensuring safe water supplies for consumption [1]. Wastewater can be categorized into municipal wastewater, agroindustrial wastewater, anaerobic digestion wastewater, metal-containing wastewater, textile wastewater, and pharmaceutical-based wastewater, depending on the wastewater treatment methods. Conventional treatment methods have several problems, such as large amounts of required energy, large required areas of land, and high operation and maintenance costs [1,2]. Algae offer an alternative treatment approach for the removal of pollutants as nutrients, while simultaneously converting these into biomass. Some species of algae have the ability to take up other pollutants, such as HMs, nitrogen compounds, and harmful chemicals. It has been reported that algae can remove nitrogen and phosphorus from municipal wastewater, achieving very low concentrations of 2.2 and 0.15 mg L−1, respectively, and convert these nutrients into biomass [3]. Prior research suggested that nutrient-rich wastewaters, containing high levels of organic carbon (COD), such as industrial and agriculture wastewater, typically undergo a dilution strategy, or anaerobic pretreatment, to avoid algal growth inhibition, caused by high COD concentration [4–6]. Chlamydomonas reinhardtii have also been reported to achieve significant Pb removal (380.7 mg g−1) [7]. Abargues et al. demonstrated that 4-tert-octylphenol, technical-nonylphenol, 4-nonylphenol, and ­bisphenol-A in Anaerobic Membrane BioReactor effluents can be efficiency removed via microalgae [8]. In addition, algae offer advantages of high growth rate, high lipid yield, high environmental tolerance, low competition for arable land and potable Biomass, Biofuels and Biochemicals. https://doi.org/10.1016/B978-0-444-64192-2.00008-1 © 2019 Elsevier B.V. All rights reserved.

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CHAPTER 8  Algal culture and biofuel production using wastewater

­ ater, and no noticeable seasonal limitations on culturing [9]. A schematic presentaw tion of algae-mediated wastewater treatment, with simultaneous biomass production for the biofuel generation, is shown in Fig. 1. Several scientists have demonstrated that algae cultivation using various wastewaters is, compared to traditional methods, a more effective and economic way to reduce biomass production costs. It also, notably, provides the extra benefits of simultaneous wastewater treatment [6,10,11]. Generally, in wastewater-systems, algae grow together with bacteria. Bacteria can efficiently oxidize the COD, in combination with CO2 generation. Algae can convert CO2 to biomass via photosynthesis, and O2 will be produced to promote bacterial growth (Fig. 2). Thus, wastewater can be treated well by the algae-bacterial consortium system without additional oxygen supplementation. At the same time, nutrients can be converted into biomass, and the CO2 emission into the atmosphere will be reduced. In addition, senescent and dead algal residues are abundant sources of organic compounds, as dissolved organic matter (DOM), by aggregate associated bacteria [12]. Additionally, nitrogen from the wastewater is removed, due to the assimilation of ammonium into the algal biomass, or when algae take up nitrogen in the form of nitrate. As a result, regardless of the nature of the growth media (i.e., wastewater), the algae biomass can be estimated by considering photosynthesis energy, respiration energy, and nitrogen uptake energy [13].

FIG. 1 Schematic presentation of simulations of wastewater treatment with microalgae biomass cultivation for biofuel generation.

2 ­ Selection of algae species used for wastewater treatment

FIG. 2 Nutrient and energy flow in microalgae-bacteria consortium.

As an advanced method of water treatment, algae are cost-effective and sustainable, while at the same time, producing commercially valuable products. The nutrient removal efficiency of algae is higher than that of other microorganisms, because algae can utilize the nutrients (ammonia, nitrate, phosphate, and trace elements) that are present in various wastewaters. The development of open and closed systems of microalgal cultivation, coupled with wastewater treatment, has led to an improvement in algal biomass production. Overall, algae cultivation is an efficient method to remove pollutants from wastewater and to acquire the energy for growth. This review mainly analyzes strategies for strain selection, the effect of wastewater types, photobioreactor design, and the potential of algae-bacteria consortium treatment, using wastewater for promoting both algae-based biofuel production and wastewater treatment, to achieve the ultimate goal of commercialization.

2 ­SELECTION OF ALGAE SPECIES USED FOR WASTEWATER TREATMENT Since blue-green algae, diatoms, flagellate algae, and green algae were identified as the four groups of algae genera found in wastewater stabilization ponds in the 1970s, algae that can be used to treat wastewater have been broadly studied [14,15]. It is essential to select algae for use in wastewater treatment the potential for higher growth rate, higher lipid/starch production, higher CO2 and NH4+ tolerance, higher tolerance to the pollution of metal ions (e.g., Cd, Cu, Pb, and Cr) and organic matter (e.g., acetate, butyrate, and propionate), and robust growth properties against a variety of severe environmental conditions [16]. These criteria are vital, and algal growth has been reported as the main reason for limiting the increase of nutrient and pollutant removal efficiency of an algae-bacteria consortium.

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Knowledge about the indigenous species in specific wastewaters can form a basis for selecting the species of algae, since the particular characteristics of such algae can be an advantage. Several algal species, such as Chlorella [6,17], Scenedesmus [18], Desmodesmus [19], Neochloris [11], Chlamydomonas [20], Nitzschia [21], and Cosmarium [22] have been applied in various wastewater treatment types, coupled with biofuel production, under both sterilization or nonsterilization conditions [16]. Among them, the species of Chlorella, Scenedesmus, and Cyanobacteria were most commonly employed, in various wastewater treatments [6,23–26]. For instance, it has been reported that Chlorella sp. has a particularly high tolerance for VFAs, TN, TP, COD, and CO2, making it suitable for wastewater [27]. Scenedesmus can be cultivated in high saline, piggery wastewater [26], or high COD-loading, swine wastewater [28]. Moon et al. reported that the lipid content of C. reinhardtii increased with the addition of acetate [29]. A type of green freshwater microalga, Botyrococcus braunii, is famous for its ability to constitutively synthesize and store high quantities of many types of lipids [30]. Chinnasamy et al. used wastewater from the carpet industry as a nutrient source to cultivate B. braunii, achieving a biomass of 340.4 mg L−1 d−1 and a lipid productivity of 13% [2]. In addition, Yang et al. reported that the lipid content of Chlorella minutissima UTEX2341 was improved by 21% and 94%, respectively, by adding 1.0 mM Cu and 0.4 mM Cd, suggesting that small amounts of trace metals have the ability to induce lipid synthesis [31]. Some macroalgae, such as Sargassum cymosum, have the beneficial ability of HMs bio-adsorption or bio-accumulation, such as Cu, Pb, and Ge [32]. Some brownmacroalgae (e.g., Ascophyllum nodosum, Fucus spiralis, Laminaria hyperborea, and Pelvetia canaliculata) showed potential of transition metal removal from petrochemical wastewaters [33]. These observations can be utilized as a guideline for choosing a specific microalgal strain for a particular purpose. The choice of algae for wastewater treatment is primarily based on the pollutants the algae need to deal with. In other words, for different sources of wastewater, the mechanisms of wastewater treatment by algae should differ [16]. As shown in Fig. 3, based on different wastewater sources, the mechanisms of algal wastewater treatment can mainly be divided into bio-adsorption, bio-accumulation, bio-coagulation, and bio-conversion, which will be critically reviewed in the following section.

3 ­POTENTIAL OF AN ALGAE-BACTERIA CONSORTIUM SYSTEM USED FOR WASTEWATER TREATMENT Algae-bacteria associations can drive aerobic processes that can be regarded as a feasible wastewater treatment method (Table  1). It has been reported that the cell growth of algae can be enhanced when algae are cultivated together with bacteria, and in nature, algae and bacteria are widely known to form consortia [45]. The formation of such an algae-bacteria consortium is dynamic, and can be divided into four processes: (1) The algae-bacteria consortium is promoted by the presence of extracellular polymeric substances (EPS), due to bridging of the large superficial area

3 ­ Potential of an algae-bacteria consortium system

FIG. 3 Mechanisms of various wastewater treatments using microalgae and bacteria.

of activated bacteria flocs. (2) Attachment of the nascent bacteria onto the surface of algae, mainly to the phycosphere on the surface of algal cells and its immediate environs. (3) Algae and bacteria are evenly distributed in particles, accompanied by the growth of both species of biota. (4) Formation of a dynamic balance between biomass attachment and detachment, which is considered to be synergistic between algae and bacteria [6]. The extraordinarily high biodiversity in the algal-bacterial consortium supports complex interactions between algae and bacterial groups, such as cooperative interactions that promote the growth of both algae and bacteria, and competitive/­antagonistic interactions of nutrients and space [46,47]. Cooperative biotic interactions between algae and bacteria are important for microbial metabolism and growth, as well as for the pollutant removal capacity and ecological functions. Algae can provide a carbon source for bacteria, through the decomposition of organic matter, while algae and bacteria co-exist symbiotically via the exchange of CO2 (from bacterial respiration) and O2 (from algae photosynthesis) [13]. An algae-bacteria consortium system has several advantages: (1) Co-cultivation not only reduces the otherwise high costs, but also decreases the spatial distance for the exchange of O2 and CO2, compared to separated culture units. (2) The starvation term leads to better removal efficiencies of COD, nitrogen, and phosphate. (3) Biomass and lipid productivity are enhanced. (4) The settle-ability is increased, compared to a pure algae system, making it easy to harvest or remove [16,47]. Nutrient exchange has been considered as the most common type of interaction for algal/bacterial interactions in the natural environment. Ramanan et al. reported

171

172

Pollutant removal Strain

Wastewater

COD (%)

Nitrogen (%)

Phosphorus (%)

Chlorella vulgaris + activated sludge

Synthetic wastewater

83.6

89.4

91.4

Consortium of algae, consisting primarily of Chlorella (95.2%), Chlamydomonas (3.1%), and Stichococcus (1.1%) + bacteria Chlorella vulgaris + Enterobacter asburiae Chlorella vulgaris + Klebsiella sp. Chlorella vulgaris + Raoultella ornithinolytica Selenastrum sp. + bacteria

Anaerobically digested swine manure

NA

NA

90

Synthetic wastewater

95.0 ± 0.7

100 ± 0

Synthetic wastewater Synthetic wastewater Composting leachate liquids Municipal wastewater

85.6 ± 3.8

Municipal wastewater

Chlorella vulgaris + Pseudomonas putida Chlorella vulgaris + activated sludge

Note

Reference

Settle-ability increasing compared with pure microalga Photo-sequencing batch reactor (PSBR); organic carbon source

[34]

96.2 ± 1.4

Bacteria: activated sludge native bacteria

[36]

97 ± 4.8

95.6 ± 2.2

[36]

89.4 ± 2.9

100 ± 0

95.8 ± 2.1

NA

>90

92

97

100

100

10R: about 55

0.5R: 95

0.5R: 100

Bacteria: activated sludge native bacteria Bacteria: activated sludge native bacteria Diluted biowaste leachate (1%) Remove NH4+-N and PO43−-P completely within 18 h R = activated sludge/Chlorella vulgaris

[35]

[36] [37] [38]

[39]

CHAPTER 8  Algal culture and biofuel production using wastewater

Table 1  Different consortia of algal-bacteria used in wastewater treatment

Municipal wastewater

92.3

95.7

98.1

Chlorella vulgaris + Pseudomonas putida

Synthetic wastewater

85.5

85

66

Chlorella vulgaris + Bacillus licheniformis

Synthetic wastewater

86.55

88.95

80.28

Microcystis aeruginosa + Bacillus licheniformis

Synthetic wastewater

65.62

21.56

70.82

Chlorella sp. + activated sludge

Synthetic wastewater

87.3

99.2

83.9

Algal + bacteria

Synthetic wastewater

96.0

46.0

45.7

NA, not available.

Bacteria: Flavobacteria and Sphingobacteria Co-culture of immobilized C. vulgaris and suspended P. putida Chlorella vulgaris + Bacillus licheniformis ratio is 1:3 Microcystis aeruginosa + Bacillus licheniformis ratio is 1:3 Pseudomonas putida and Flavobacterium hauense were enriched in sludge when cultured with algae in light Bacteria: the predominant families covered Actinobacteria, Bacteroidetes

[40]

[41]

[42]

[42]

[43]

[44]

3 ­Potential of an algae-bacteria consortium system

Scenedesmus sp. + Bacteria group

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that organic matter is decomposed by bacteria into its mineral form, and secretes extracellular metabolites, such as auxins and vitamin B12, which are essential for microalgal growth [48]. Nitrogen is a further important element, and nitrogen-fixing cyanobacteria are key organisms in the nitrogen-mediated interaction of aquatic ecosystems. Some of these cyanobacteria live symbiotically in the host of the eukaryotic algae, and have adapted to this symbiotic interaction with their host at the genomic level [49]. Nitrogen-mediated interactions were also reported between algae and heterotrophic bacteria; screening of growth-promoting bacteria for the microalga Dunaliella has suggested the possibility that some bacteria facilitate nitrogen assimilation via microalgae [50]. Su et al. reported that assimilation of nitrogen into biomass accounted for 61%– 93% of nitrogen removal in batch reactors with an algal-bacterial consortium [51]. Furthermore, addition of Brevundimonas sp. to Chlorella ellipsoidea prolonged its exponential growth phase, resulting in a 50-fold increase in biomass yield, and Brevundimonas sp. experienced a second exponential growth phase, giving a 5-fold increase in cell densities, compared to those achieved in monoculture [52]. Scenedesmus sp. was co-cultured with indigenous municipal wastewater bacteria for the treatment of pretreated municipal wastewater, and the resulting biomass productivity and lipid productivity were 282.6 and 71.4 mg L−1 d−1, respectively [53]. A similar co-culture of Chlorella sorokiniana and aerobic bacteria in primarily treated potato industry wastewater, with alternate light and dark cycles, yielded a biomass productivity of 26 mg L−1 d−1, with a lipid content of 30% DW [43]. Moreover, extracellular organic matter was frequently produced in algal-bacterial consortia. Starvation has been confirmed to facilitate lipid accumulation, bacterial aggregation, and EPS stimulation, as well as the cell aggregation of algae [54]. EPS stimulation increased the settle ability of biomass, and reduced the processing costs for biomass harvesting via its highly charged polymer structure. The increased extracellular organic matter that originated from stored starch could play a central role in the flocculation of biomass, due to its highly charged polymer structure [55]. Several studies have indicated that the higher algae harvest may contribute to bacterial quorum-sensing molecules. Zhou et  al. reported that Chlorophyta sp. self-aggregated in 200 μm bio-flocs, by secreting 460–1000 kDa aromatic proteins upon interacting with N-acylhomoserine lactones, and the settling efficiency of Chlorophyta sp. reached a maximum of 41% [56]. Therefore, the algae-bacteria consortium can significantly reduce the cost of wastewater treatment, due to an efficient pollutant removal rate, high biomass and lipid productivity, and the comparatively low price of microalgal harvest, and has good application prospects.

4 ­DIFFERENT WASTEWATER TREATMENTS BY ALGAE 4.1 ­MUNICIPAL WASTEWATER Increasing urbanization, and the expansion of urban populations, has resulted in increased quantities of municipal wastewater. Municipal wastewater has few nitrogen

4 ­ Different wastewater treatments by algae

and phosphorus, but increased amounts of HMs such as Pb, Zn, and Cu. The traditional municipal wastewater treatment process includes three stages: a primary, a secondary, and an advanced stage. The removal of dissolved inorganic components, including nitrogen and phosphorus, happens during the advanced treatment process, via a number of different unit operations, including ponds, postaeration, filtration, carbon adsorption, and membrane separation [57]. Aeration processes are particularly energy intensive, and account for 45%–75% of the net energy costs of a wastewater treatment plant. Research indicates that aerobic processes driven by ­algae-bacteria associations offer a feasible alternative for wastewater treatment. Algae produce the required oxygen that allows bacteria to remove pollutants, generating the CO2 needed by bacteria [58]. Studies suggest that Chlorophyte algae, such as Chlorella, can grow well in municipal wastewater [58]. It has been reported that Chlorella sp. has been successfully cultivated in all of the studied wastewater samples. Arbib et al. evaluated the microalgal growth rate and nutrient elimination (along with CO2 biofixation) by S. obliquus and Chlorella stigmatophora, cultured in urban wastewater at different nitrogen and phosphorus ratios, ranging from 1:1 to 35:1. The appropriate nitrogen to phosphorus ratios for achieving optimum batch biomass productivity ranged between 9 and 13 [59]. The highest dry cell weight for Calothrix sp. was 0.97 mg L−1, and the N and P removal rates from wastewater were 57%–58% and 44%–91%, respectively [60]. Algae-bacteria aggregates were studied for the treatment of municipal wastewater. Low irradiance levels promoted the formation of algae-bacteria flocs and granules, reaching the highest values of TN, total COD, and P removal of 60 ± 5%, 89 ± 3%, and 28 ± 7% [58]. Arcila et al. suggested EPS formation as a relevant factor for the overall good performance with which algae-bacteria systems treat municipal wastewater, as this favors floc and granule formation and results in high removal percentages of both organic matter and TN [58]. Therefore, the mass cultivation of algae has the ability to facilitate the uptake of N and P simultaneously with high biomass productivity.

4.2 ­PHARMACEUTICAL-BASED WASTEWATER Pharmaceutical compounds (PCs) are ubiquitous in aquatic environments, and form a severe risk for wildlife and humans [61]. Because PCs were excreted from agricultural activities, hospital effluents, industrial wastes, and domestic wastes of the pharmaceutical industry, unfortunately, many PCs have been systematically found in wastewater over the past decades [62]. To date, the occurrence of >200 different PhACs has been reported in the water body [63]. Even though the concentrations of PCs in the environment mostly range from ng L−1 to μg L−1 levels, evidence suggests that they can trigger catastrophic ecological effects on target and nontarget organisms. For example, they can change microbial communities, limit the growth of microbes, decrease the microbial activity of soil, and influence the denitrification rate of bacteria [64].

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PCs are also, typically, difficult to biodegrade, and their environmental half-life is long. Harmful concentrations of PCs in high-trophic level organisms (including humans), via bio-magnification in food chains, are evident [65]. Among these, steroid PCs (estrone, 17 β-estradiol, and 17 α-ethynylestradiol) can affect the endocrine system [66]; amine-based PCs (e.g., ranitidine, nizatidine, doxylamine, and carbinoxamine) are precursors for the production of N-nitrosodimethylamine (NDMA), which poses significant health risks to humans due to its carcinogenic properties [66]; antibiotics (macrolides, sulfonamides, tetracyclines, and quinolones) can induce genetic resistance to antibiotics in bacteria [67]. Algae are primary producers in aquatic food webs, and they are key indicators for assessing water quality, and eco-toxicity of pollutants [68]. Bioremediation of contaminated waters by mixotrophic algae is a solar-power driven, ecologically comprehensive, and sustainable, reclamation strategy [20]. The mechanisms of PC removal by algae include bioadsorption and bioaccumulation, as well as both intracellular and extracellular biodegradation (Table  2). Research indicated that the bioadsorption content of PCs by algae varied from 0% to 16.7% [73] The dead cell biomass of algae was found to adsorb approximately 10% [74], since cell walls of some microalgae and cyanobacteria are composed of polysaccharides and carbohydrates that have negatively charged groups (such as carboxyl, phosphoryl, and amine). Pollutants with cationic groups are actively attracted toward the algal surface through electrostatic interaction, thus resulting in effective biosorption [64]. Bioaccumulation is an active metabolic process for the uptake of substrates, and is driven by energy. Previous research found that algae can take up organic pollutants, along with growth nutrients, via bioaccumulation. For example, triclosan, trimethoprim, and sulfamethoxazole can be removed via bioaccumulation of green alga Nannochloris sp., and approximately 23% of radiolabeled 17α-ethinylestradiol can be accumulated by Desmodesmus subspicatus within 24 h [75,76]. Carbamazepine (CBZ) is one of the most investigated compounds of pharmaceutical industry based wastewater for algal bio-accumulation. Chlamydomonas mexicana and Scenedesmus obliquus were evaluated for the toxicity, cellular stress, and bioaccumulation stability of CBZ, and achieved a maximum of 35% and 28% CBZ removal, respectively [20]. It has also been reported that a complex mixture of therapeutic drugs (CBZ included) strongly decreases the activities of ATP synthase in Pseudokirchneriella subcapitata [20], indicating that PhACs can interfere with energy transduction in both the mitochondria and chloroplasts of algae [77]. In addition, Xiong et al. reported that some key enzymes (e.g., SOD and CAT) of phototrophic microorganisms would counteract the toxicity of reactive oxygen species (ROS), via regulation of antioxidative defense mechanisms [20], which are commonly identified as biomarker indicators [69]. The accumulated PCs in algae cells can induce the generation of ROS, which are essential signaling molecules to maintain the cellular metabolism at normal levels, and can cause severe damage to cellular components if occurring in excess [78]. Due to the negligible growth inhibition of algae in the presence of PCs, it can be deduced that PCs cannot lethally inhibit microalgal activities at their relative environmental concentrations [20]. Therefore, microalgal species can survive low

Table 2  Algae used in pharmaceutical compounds containing wastewater Species Chlamydomonas mexicana Scenedesmus obliquus C. pitschmannii M. resseri Cymbella sp. Scenedesmus quadricauda Chlorella vulgaris Scenedesmus quadricauda

Microalgae consortium Microalgae consortium Consortia of microalgae and bacteria in wastewater Microalgae consortium Consortia of microalgae and bacteria in wastewater Consortia of microalgae and bacteria in wastewater a

Carbamazepine Carbamazepine Carbamazepine Carbamazepine Naproxen Naproxen Diazinon Pharmaceutical wastewater Pharmaceutical wastewater Wastewater containing emerging contaminants Wastewater containing emerging contaminants Wastewater containing emerging contaminants Wastewater containing emerging contaminants Wastewater containing emerging contaminants Wastewater containing emerging contaminants

PCTE, physico-chemically treated effluent.

NA, not available.

Biodegradation

Note

Reference −1

35% 28% NA NA 97.1% 58.8% 94% Absorption

97% growth inhibit at 100 mg L 30% growth inhibit at 100 mg L−1 31.3% growth inhibit at 100 mg L−1 43.5% growth inhibit at 100 mg L−1 100% growth inhibit at 100 mg L−1 100% growth inhibit at 100 mg L−1 >30% growth inhibition at 40 mg L−1 Microalgae can tolerance 20% PCTEa

[20] [20] [20] [20] [69] [69] [29] [70]

NA

[71]

17%

13 psychoactive pharmaceuticals were selected for experiment 4-Octylphenol, galaxolide, and tributyl phosphate concentrations Caffeine

99%

Caffeine

[72]

15%

Ibuprofen

[72]

60%

Ibuprofen

[72]

<20%

Carbamazepine and tris(2-chloroethyl) phosphate

[72]

Up to 90%

[72] [72]

4 ­ Different wastewater treatments by algae

Chlorella kessleri

Compounds

177

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CHAPTER 8  Algal culture and biofuel production using wastewater

environmental concentrations of PCs via ROS, which can be utilized to both monitor and improve the production of related genes and the expression of signals [64,78]. Biodegradation is the most effective way in which algae remove PCs from an aqueous phase. Algae form simpler molecules by catalytically degrading complex parent compounds. Peng et al. demonstrated that 95% of the biodegradation of progesterone can be achieved by the two freshwater algae S. obliquus and Chlorella pyrenoidosa, in an aqueous medium [74]. Currently, the biodegradation mechanisms of CBZ can be described with two major pathways. The first proposed pathway (route-1) suggests the formation of EPCBZ through epoxidation, via action of the cytochrome P450 (CYP450) present in the algae [20]. CYP450 has been shown to be a complex enzyme system responsible for the biotransformation of xenobiotic compounds in algae [79]. Route-2 proposes the formation of n-OH-CBZ due to the oxidation of CBZ by the CYP450 enzyme system. However, the EPCBZ formed in route-1 is highly unstable, and likely undergoes rearrangement to form hydroxyl derivatives, n-OH-CBZ (route-2). This finding is in agreement with an earlier report [80]. It has also been reported that microalgal biodegradation prevented the formation of carcinogenic intermediates, which can be considered as a significant achievement for the microalgal biodegradation of CBZ [16]. Moreover, multiple types of EPS, including polysaccharides, protein, enzymes, substituents (polysaccharide-link methyl and acetyl groups), and lipids could be excreted by the algae into the surrounding environment. A hydrated biofilm matrix can be formed by EPS, which acts as an external digestive system, since the biofilm matrix can keep extracellular enzymes around cells and metabolize these either dissolved, colloidal, or in solid form as organic compounds. Nutrients are accumulated from the environment by the charged polysaccharides and proteins. Furthermore, the adsorption of xenobiotics by polysaccharides and proteins contributes to the desired environmental detoxification [81]. These interactions among different types of EPS, and the interactions between EPS and microalgal cells, can promote extracellular degradation of the organic compounds, such as PCs, and can also form byproducts that affect the intracellular degradation [82]. Recently, Matamoros et al. reported that the algal consortium, containing Chlorella sp. and Scenedesmus sp., can successfully remove 20% of the CBZ from urban and synthetic wastewater [72]. The removal of PCs from wastewater by an algae-bacteria consortium could either happen via bioaccumulation or biodegradation. However, the elucidation of the actually applied mechanism, and the role of bacteria in such processes, needs to be investigated further.

4.3 ­ TEXTILES WASTEWATER Textiles are one of the main traditional worldwide industries that use various commercially available dyes, producing >7 × 105 tons of dyestuffs per year worldwide [27]. Textile wastewaters contain dye, inert auxiliaries, and chemicals such as acids, waxes, fats, salts, binders, thickeners, urea, surfactants, and reducing agents. These dye effluents are highly variable in their composition, with relatively strong color,

4 ­ Different wastewater treatments by algae

high COD, high salinity, high temperature, variable pH, and low biochemical oxygen demand (BOD) [83]. Such effluents can affect both water quality and gas solubility, which adds toxicity to aquatic plants and animals, leading to severe global environmental problems. Algae are promising microbes not only to treat textile wastewater by uptaking nutrients and dyes, but by accumulating lipids that can then be transesterified into biodiesel (Table 3) [94]. Algal bioremediation of textile wastewater may happen due to two mechanisms: bioconversion, or bioaccumulation and biosorption processes. Algae also adsorb dyes onto their surface, while algae utilize dyes as carbon sources, and convert these into metabolites during the bioconversion process [94]. Algae species such as Chlorella vulagris, C. pyrenoidosa, and Oscillatoria tenuisin degrade azo dyes into simple aromatic amines, and thus decolorize dye wastewater [94]. Meng et al., studying acid red 27, achieved decolorization into less phytotoxic aromatic amines via Shewanella algae, in the presence of high concentrations of NaCl and different quinones or humic acids [95]. Moreover, an ability of C. vulgaris to break down the azo bond has been observed [96], and alga Caulerpa lentillifera have been reported to be able to remove basic dyes via bio-sorption [89]. Cheriaa et al. indicated that Chlorella alga decolorized different dyes variably, for example, indigo 89.3%, direct blue (DB) 79%, remazol brilliant orange (RBO) 75.3%, and crystal violet 72.5% [88]. Chlorella vulgaris could reduce COD up to 70% in textile wastewater [97]. During the biosorption process, both dead and living algae can participate, due to their organic function groups and surface area [98]. For instance, reactive red 120 (RR-120) can be removed from its aqueous solution by Spirulina platensis, reaching a maximum biosorption capacity of 482.2 mg g−1 [99]. The removal of malachite green (MG), and methylene blue (MB), has been reported using the biomass of Desmodesmus sp. [88]. It has also been reported that the algal dye adsorption efficiency is highly correlated with the dye concentration in the wastewater. This was found by using the green seaweed C. lentillifera as biosorbent [89]. To further understand the mechanism of algal biosorption, the related adsorption equilibria were applied for evaluating the adsorption type. Langmuir, Freundlich, Langmuir-Freundlich, and Koble-Corrigan adsorption models were employed for the mathematical description of biosorption equilibria, together with evaluating the isotherm constants at different temperatures [87]. Algal cell walls present organic functional groups associated with polysaccharides, alginic acid, and proteins for binding various pollutants. The adsorption of reactive dyes (e.g., Remazol Red and Remazol Golden Yellow) via the dried biomass of C. vulgaris followed the Langmuir model [87], suggesting that the dyes were adsorbed on a monolayer coverage on homogenous sites of the algal cell wall. However, reference to the Freundlich model indicates the existence of a heterogeneous surface, with sorption sites of different affinities [6]. A novel photo bio electrochemical system (PBES) was constructed by shaking down the algal-bacterial biofilm at both anode and cathode, and applying C. vulgaris and indigenous wastewater bacteria as inoculums [100]. The successful operation of PBES is achieved due to the synergy between C. vulgaris and mixed

179

180

Species

Compounds

Mechanism

Note

Reference

Chlorella pyrenoidosa

Methylene blue

Adsorption

[84]

Chlorella sp. Chlorella sp. Spirulina platensis Chlorella pyrenoidosa Desmodesmus sp.

Methylene blue Methyl orange Reactive blue 19 Direct red-31diazo dye Methylene Blue and Malachite Green Blue dye Blue dye Red dye Red dye Dye Dye Methylene blue RGB-RED dye Congo red dye

Degradation Degradation Adsorption Degradation Adsorption

Dry biomass of algae showed higher adsorption capacity (21.3 mg g−1) compared to wet algal biomass (20.8 mg g−1) 23% color removal >70% color removal Algae adsorption capacity is 251.61 mg g−1 96% color removal 98.3% color removal

Degradation Degradation Degradation Degradation Degradation Degradation Adsorption Degradation Adsorption

78.29% color removal 76.48% color removal 64.21% color removal 62.63% color removal 93% color removal >75% color removal 98.9% color removal 95% color removal 82.6% color removal

[89] [89] [89] [89] [90] [91] [92] [93] [93]

Spirogyra sp. Oscillatoria sp. Spirogyra sp. Oscillatoria sp. Chlorella vugaris Chlorella sp. G23 Laminaria japonica Nostoc muscorum Spirulina platensis

[85] [85] [86] [87] [88]

CHAPTER 8  Algal culture and biofuel production using wastewater

Table 3  Algae used for textile dye removal from wastewater

4 ­ Different wastewater treatments by algae

bacteria. This system is a promising way to treat wastewater that contains azo dye. It could enhance azo dye degradation, and possesses both high net power output and buffer minimization [100]. Additionally, various dye wastewaters can be cleaned by different species of algae The ability of C. vulgaris, Lyngbya lagerlerimi, Nostoc lincki, Oscillatoria rubescens, Elkatothrix viridis, and Volvox aureus to decolorize and remove methyl red, orange II, G-Red (FN-3G), basic cationic, and basic fuchsin, has been investigated [101].

4.4 ­METAL-CONTAINING WASTEWATER Metal-containing wastewater originates from metal plants, battery manufacturing, mining activities, tanneries, and petroleum refineries [96] that utilize HMs (or chemicals containing HMs) in their industrial processes. These processes result in the generation of wastewaters that contain HMs, which are discharged into the surface water. HMs are among the most severe pollutants, which could significantly jeopardize human health and ecological systems, due to their toxic and nonbiodegradable characteristics. It has been reported that various toxic and carcinogenic HMs such as Pb, Cu, Cd, Ni, Zn, and Cr may cause severe human health problems, and need to be removed from the environment [102]. Many studies have clearly demonstrated the potential of HM removal from wastewater via algal biomass [103–106]. The phenomenon of algal remediation could also be broadly divided into two categories: bioaccumulation by living cells, and biosorption by nonliving, nongrowing biomass or biomass products [107]. For living algal cells, biosorption of HMs is a complex process. However, Monteiro et al. indicated that accumulation of HMs by algae typically comprises a two-stage process: (i) the initial rapid removal of HMs at the cell surface, and (ii) a much slower process that occurs within the cell [108]. The first process, the passive removal, is nonmetabolic, rapid, and essentially reversible, and occurs in both living and nonliving cells. Here, HMs are adsorbed onto both cell surfaces and extracellular polysaccharides via tightly binding to the organic functional groups of algae, with the adsorption mechanism of physical adsorption, ion exchange, electrostatic adsorption, chemisorption, coordination, complexation, chelation, microprecipitation, entrapment in the network of structural polysaccharides, and diffusion through both cell wall and membrane [108]. The second phase is metabolism-dependent, and includes transporting HMs through the cell membrane barrier and subsequently accumulating inside the cell, with posterior binding to intracellular compounds and/or the organelle containment. This process of HM uptake is slow and typically irreversible, and only restricted to living algal cells. Moreover, specific proteins mediate the transport of HMs through the partially lipophilic biological membrane that surrounds the cell, since most of the HMs are hydrophilic [64,108]. Dried biomass from algae can also be applied to remove HMs from wastewaters as cation exchanger, and metals can be subsequently recovered via desorption with acids or other desorbing agents [83]. Very efficient removal of Cu (80%) and Cd (100%) from wastewater, with a maximum removal rate within 5 min after contact,

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was observed with a mixture of dried biomass [109]. Zheng et al. indicated that the lipid extraction residue from the strain of Coelastrum sp. PTE-15 had the highest capacity of Cd sorption (32.8 mg g−1), due to the negative charge of functional groups located in the alginate of the microalgal cell wall [110]. In the algae-bacteria consortium system, the acidic functional groups of bacterial cell walls can also bind significant concentrations of aqueous cations, which can affect the speciation, distribution, and mobility of these cations [106]. C. sorokiniana and R. basilensis were found to metabolize salicylate, with a subsequent removal of HMs from the solutions [111]. The consortium system removed Cu more efficiently than the individual organisms, suggesting a specific linkage between bacterial and algal species [112]. Future research for algae-bacteria consortium based HMs removal should, therefore, address the following points: (1) The mechanism of algae-bacteria consortium for HMs removal, such as biosorption, bio-convention, or bioaccumulation, should be systematically investigated; (2) the synergistic effects of algae and bacteria require further investigation; (3) ecological cation-exchangers can be developed, since dried biomass of algae and bacteria possess a good ability of ion exchange due to charged cell walls.

4.5 ­AGRO-INDUSTRIAL WASTEWATER Agro-industrial wastewaters, which are rich in organic matter, TN, and TP nutrients, mainly include swine/dairy manure wastewater [6,113], palm oil mill effluent (POME) [114], and runoff and drainage water from agricultural lands [115]. Wang et al. reported that the carbohydrate-rich microalga C. vulgaris JSC-6 can efficiently remove 60%–70% COD, and 40%–90% NH3-N, from swine wastewater [6]. C. vulgaris was also reported as a successful bioremediation agent for POME, achieving reductions of ammonia-nitrogen, phosphorus, COD, and BOD of 61%, 84.0%, 50.5%, and 61.6%, respectively [116]. Moreover, Cheah et al. indicated POME as effective for algae cultivation and causing high lipid accumulation [117]. In the farming system, N and P from fertilizers, which has sufficient capacity to support algal growth, may be lost via runoff or leaching pathways [115]. A previous study demonstrated that agro-industrial wastewaters need to be digested or diluted before algae cultivation due to higher nutrient concentration [118]. Mulbry et al. reported that Rhizoclonium sp. was able to grow in raw and anaerobically digested dairy and pig manure, at loading rates of 0.2–1.3 g TN m−2 d−1 for swine manure, and rates of 0.3–2.3 g TN m−2 d−1 for dairy manure [113]. It has also been reported that S. platensis can remove 90% of COD from anaerobically digested POME [119]. Chlorella sp. cultivated in 20% of POME with 40% synthetic nutrients reached the highest lipid productivity of 34 mg L−1 d−1 [120]. In addition, high ammonium concentration is a common characteristic of agroindustrial wastewaters, which is highly correlated to eutrophication [6]. Fortunately, many species of algae can grow well in “nutrient-rich” environments, and convert the nutrients that are contained in agro-industrial wastewaters to biomass rapidly [6,121]. For instance, Neochloris oleoabundans, C. vulgaris, and S. obliquus were

4 ­ Different wastewater treatments by algae

cultivated and compared for nitrogen removal ability and algal lipid production in agro-zootechnical digestate [122]. Under optimal conditions, ammonium was efficiency removed by algae, reaching rates above 90% [6,123]. Ayre et  al. suggested that algae have the ability to grow at up to 1600 mg L −1 NH4+-N over five weeks, through a semi-continuous strategy [124]. Moreover, cyanobacteria, such as Oscilatoria, Anabaena, and Spirulina are able to utilize elemental nitrogen as their sole nitrogen source, via reduction of N2 to ammonium [125]. In general, cyanobacteria prefer to utilize ammonium rather than nitrate, because the uptake of nitrate relies on light [126]. Thus, a combination of algae and cyanobacteria for ammonium-rich agro-industrial wastewaters would be a potential solution. Uptake of nitrate would be limited by high concentrations of ammonium, because the synthesis of nitrate reductase is repressed by ammonium, while ammonia uptake is inhibited by elevated nitrate concentrations [127,128]. Furthermore, high temperatures can promote the formation of free ammonia, which is generally harmful for photosynthetic organisms [129]; however, this toxicity appears to diminish in alkalophilic species such as S. platensis [130].

4.6 ­ ANAEROBIC DIGESTION WASTEWATER Anaerobic digestion is one of the most widely-applied biological processes that can efficiently convert waste activated sludge to bioenergy (e.g., H2 and CH4) [131]. However, AD by-products (including residues and effluents) are considered an environmental threat, because AD effluents possess high COD, TN, and TP [132]. In addition, the obtained biogas typically contains approximately 20%–60% CO2, and 3000–5000 ppm H2S, which is not favorable as fuel gas without prior purification [133]. Thus, developing a low-cost strategy to treat AD effluent and upgrade the quality of biogas to meet the practical demand is urgently required. Due to their high growth rate, superior environmental adaptability, and great nutrient-removal ability, algae are regarded as a feasible means to convert effluent wastes (e.g., TN, TP, and VFAs) to biofuels (e.g., biodiesel) [134]. During microalgal cultivation, CO2 can be converted to biomass via photosynthesis [135]. Through the Calvin cycle, CO2 can be converted into sugars and glyceraldehyde 3-phosphate (GAP), which is the primary precursor for the synthesis of triacylglycerol (TAG) and can be accumulated under environmental stress [136]. Algae which tolerate high CO2 and CH4 concentrations are preferred. Chlorella sp. can increase the CO2 tolerance levels via random mutagenesis [3]. The mutant Chlorella sp. MM2 can tolerate up to 80% of CH4 [137], while a native strain of Nannochloropsis gaditana can tolerate 100% CH4, without any significant changes in growth or biomass production [138]. In addition, the H2S concentrations in biogas can affect microalgal growth because dissolution of H2S would reduce the pH of algae cultivation. Hence, H2S-tolerant strains should be used. Scenedesmus sp. was reported to tolerate up to 3000 ppm of H2S [28]. The H2S content needs to be lowered before introducing the biogas into the algae culture [133,139], whereas some algae species are able to upgrade biogas by using raw biogas that is rich in H2S [28,140].

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Algae can transport and metabolize VFAs efficiently, albeit in a hierarchical manner. Furthermore, acetate is carried into the cellular glyoxysome, where it is converted into acetyl-CoA catalyzed via acetyl-CoA synthetase in the chloroplast, and is then incorporated into long-chain acyl-CoA along with free fatty acids [141]. AcetylCoA is the molecule that attaches to the glycerol backbone and participates in the Kennedy pathway for TAG synthesis [142]. Ramanan et al. showed that addition of acetate to algae under N-limitation could promote the expression of the ACS gene in the lipid synthesis pathway, and thus promote lipid accumulation [141]. Acetyl CoA is also converted from butyrate via Crotonyl CoA in the glyoxysome. Furthermore, it has been reported that the energy produced by the butyrate metabolism can compensate for the energy consumed by the transport of butyrate, leading to no net energy gain [143]. Butyrate that will be inhibited when above 0.1 g L−1 is used as the sole carbon source [144]; however, when it is present with other VFAs, it can be consumed by algae in a diauxic pattern [145], particularly with a higher acetate to butyrate ratio [146] or at higher substrate to microorganism ratios [144,147]. The other major VFA (propionate) can be converted to either acetyl CoA or succinyl CoA and utilized by algae [148], but it cannot support its growth as the sole carbon source as well [149]. Heterotrophic growth of C. protothecoides has been reported to preferentially use valerate and isovalerate [150,151]. Lactate was reported to inhibit the growth of C. vulgaris at concentrations above 0.5 g L−1 [144], but it can be consumed in a diauxic pattern [144,145,152]. Since both preference and utilization of VFAs seem to differ for different species, it would be favorable to effectively utilize and remove all VFAs present in the anaerobic effluents via the algal consortium. For instance, butyrate and propionate are not good for the growth of axenic algal strains, while butyrate and propionate as sole carbon source could be satisfactorily assimilated by establishing an algal consortium [153]. In summary, under mixotrophic conditions, GAP and acetyl-CoA pools will be dramatically enhanced by the dual carbon sources of CO2 and extra cellular organic carbons (i.e., VFAs), which is beneficial for algal biomass production and lipid accumulation. Moreover, there is other nutrition in anaerobic effluent. Because the nitrogen source produced from sludge digestion is mainly NH4+, selection of a microalgal strain with high growth rate and high NH4+ fixation efficiency, while also developing a cultivation strategy that can improve both biomass production and lipid accumulation, is urgently required. Several trace minerals have been investigated for their capacity to enhance lipid accumulation in algae [154]. In general, the sludge-digested broth contains various trace metals, which may be beneficial for microalgal growth. It has been reported that a small amount of Fe addition helps in sludge pretreatment [155]. This can be regarded as the main metal affecting the efficiency of both PSI and PSII, nitrogen simulation, respiration, and DNA synthesis and thus, helps not only cell growth but also lipid accumulation in algae [156]. The concentrations of Mg2+ regulate the fate of key metabolites (e.g., GAP) and thus, further influence the accumulation of TAG [157]. Above all, combining the sludge fermentation and algae cultivation is theoretically applicable and should be

5 ­ Design of photo-bioreactors for algal wastewater treatment

further investigated. The microalgal biological process associated with cell growth, metabolism, and the uptake of ions is influenced by the pH value [158]. When using sludge-digested broth to cultivate algae, the pH will sharply change, due to its insufficient buffer effect. The exhaustion of organic acids further changes the pH value, which inhibits the cell growth and lipid synthesis in algae [142]. Consequently, to combine this with a sludge-digestion tank, it is necessary to develop a pH-­controllable microalgal cultivation system.

5 ­DESIGN OF PHOTO-BIOREACTORS FOR ALGAL WASTEWATER TREATMENT To enhance economic feasibility and operational stability, an appropriate scaling up of the algae cultivation system is required. Currently, most of all algal bioreactors are suspended cultures, which can be classified into open and closed systems (Table 4). The open pond culture system is generally regarded as the most economical process among algae cultivation systems, due to low operating costs and simple operation. The types of open pond systems can be categorized into slope systems, raceway ponds, and circular ponds, which have been developed for decades. Gonzalez et al. indicated that oxidation of both organic matter and ammonium can be achieved by a C. sorokiniana-mixed bacterial culture from the activated sludge process in a tubular biofilm photobioreactor [162]. A high rate algal pond (HRAP) has high efficiency rates for removal of COD and TP. The maximum biomass production obtained by an algae-bacteria consortium under all experimental conditions was 12.7 g of volatile suspended solids (VSS) m−2 d−1 [121]. Gutiérrez et al. reported that microalgal biomass production ranged between 3.3 and 25.8 g TSS m−2 d−1, depending on the weather conditions. Furthermore, biomass recycling had a positive effect on harvesting efficiency, and enabled higher biomass recovery (92%–94%) in the HRAP with recycling (R-HRAP), than in a control HRAP without recycling (C-HRAP) (75%–89%) [163]. The major limitations of open pond culture systems are low productivity, due to the natural environment, and contamination. The use of highly selective culture conditions can reduce contamination with protozoa and other algae. This restricts suitable species for open pond cultivation. For instance, C. vulgaris needs a nutrient rich medium, Duniella salina is suitable for high salinity, and Spirulina achieves good growth under high alkalinity [164]. The advantages of a closed system have been widely reported, and include high CO2 fixation rate, high cell growth rate, low contamination risk, and controllable hydrodynamics [165]. The most popular photobioreactor configurations are tubular, vertical or column, flat plate, and annular reactors [164]. Anbalagan et al. ­investigated an indigenous microalgal-bacterial consortium, in a pilot tubular interconnected photobioreactor, to remove CO2 and toluene, using diluted centrate in seawater as a free nutrient source. The photobioreactor supported steady-state nitrogen and phosphorus removals of 91 ± 2% and 95 ± 4%, respectively, using 15% diluted centrate [166].

185

186

Type Hollow fiber membrane

Strain

Nitrogen removal

Note

Reference −1

Chlorella vulgaris + Pseudomonas putida Microalgae + bacteria

NA

Biodegradation of 500 mg L glucose using oxygen from microalgae.

[159]

Below 0.01 mg L−1 in effluent

[160]

Photo-sequencing batch reactor (PSBR) Sequencing batch reactors (SBR)

Chlorella + bacteria

90%

Dominate microalgae: Chlorella, Oocystis and Scenedesmus. Dominate bacteria: Aulacoseira, Stephanodiscus, Diatoma, Cryptophyceae and Melosira Without aeration

Microalgae + activated sludge

35%

[161]

High rate algae ponds

Microalgae-bacteria consortia

80%

Combined photobioreactor and electrocoagulation process to removal total nitrogen in the effluent Slaughterhouse wastewater, working volume 75 L

Tubular biofilm

[35]

[121]

CHAPTER 8  Algal culture and biofuel production using wastewater

Table 4  Photo-bioreactors used in algae-bacteria wastewater treatment

6 ­ Conclusion and perspectives

Immobilized culture systems include matrix-immobilized systems and biofilms. In recent years, research has increasingly focused on utilizing biofilm reactors for algae cultivation, to achieve better performance during algae-based wastewater treatment, in contrast to conventional suspended cultures. The EPS produced by algae consists of polysaccharides, proteins, nucleic acids, and phospholipids, which can also help to establish the biofilm [167]. Biofilm-based culturing is the most common immobilized culture system, and is promising for increasing the algal culture density with lower water and land requirements [16]. This has obvious advantages for biomass and lipid/carbohydrate production, nutrient removal, and lower energy cost compared to suspended culture photo-bioreactors (e.g., tubular photobioreactor and plate photobioreactor). It has been reported that algae biofilm reactors may have advantages for biomass and lipid production, nutrient removal, and energy cost [168]. A vertical-algal-biofilm-enhanced raceway pond (VAB-enhanced raceway pond) was designed and assessed for both wastewater treatment and algal biomass production. The results indicated a maximum removal capacity of the system of 7.52, 6.76, and 0.11 g m−2 d−1 for COD, TN, and TP, respectively [169]. Vu and Loh used a hollow fiber membrane photobioreactor (HFMP) to cultivate microalgae and bacteria in wastewater treatment. This study demonstrated the symbiotic relationship, as reflected by the photoautotrophic growth of C. vulgaris using CO2 provided by P. putida, and biodegradation of 500 mg L−1 glucose by P. putida utilizing photosynthetic O2 produced by C. vulgaris [159]. The rotating algal biofilm reactor (RABR) as the tertiary treatment process and using mixed culture, showed excellent algal biomass production (31 g m−2 d−1) [170]. Compared to the RABR, the algal biomass production of horizontal biofilm reactors using municipal wastewater effluents was less, but higher C, N, and P was removed from the wastewater [171]. The enclosed biofilm photo-bioreactors are economical, and their achieved nutrient removal efficiency is high (99% ammonium, 86% phosphorous, and 75% total COD). A hybrid bioreactor that simultaneously supports heterotrophic and autotrophic microorganisms was proposed by Wu et al., for the removal of high-loading nutrients; this system achieved efficiencies of about 81% of TP and 86% of ammonium [172]. Raceway ponds, flat-plate, tubular PBR, and algal biofilm PBR were compared by Ozkan et  al., in terms of algal biomass production and energy efficiency. The biofilm PBR provided the highest algal biomass concentration (96 g L−1), followed by the flat PBR (2.7 g L−1), tubular PBR (1 g L−1), and raceway pond (0.35 g L−1) [173]. Therefore, an algae immobilized system is not only applicable for simultaneous COD and nutrients removal, but it will also be easier and less expensive to collect or harvest the microalgal cells from biofilms for further uses.

6 ­CONCLUSION AND PERSPECTIVES Both algae, and algae-bacteria consortia, can be successfully applied to treat municipal wastewater, agro-industrial wastewater, anaerobic digestion wastewater, metalcontaining wastewater, textile wastewater, and pharmaceutical-based wastewater.

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The algae convert part of the nitrogen/phosphate, organic carbons, VFAs, pharmaceutical compounds, dye compounds, and HMs into biomass and biofuels, thus forming a feasible and reliable process for the dual purposes of waste reduction and biofuel generation. In addition, such an algae-bacteria consortium can significantly increase the efficiency of the achieved pollutant removal rate, increase biomass and lipid productivity, and lower the price of microalgal harvest, indicating good prospects of practical application. This study indicates that bioadsorption and biodegradation are the main mechanisms of pollutant removal in algae cultivation systems.

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