Abstract

Flocculation is a common technique to harvest microalgae, where the negatively charged algal cells coalesce together to form larger flocs that settle under gravity. Although several inorganic flocculants have been applied for algal biomass recovery, the dosage varies depending on the algal strain-specific features. Thus, the selection of inorganic coagulant that can be applied at a low dosage for achieving the maximal biomass recovery under normal physiological conditions is necessary. The present study analyses the influence of different inorganic flocculants like ferric chloride (FeCl3), alum, calcium hydroxide, ferrous sulphate and copper sulphate on the biomass removal efficiency of a mixed microalgal consortium isolated from the open ponds of the National Institute of Technology Rourkela and further enriched with diluted human urine. Flocculation experiments were carried out with varying coagulant dosages, pH between 7.5 and 7.8, and 0.5 g L−1 algal concentration. The results revealed that FeCl3 at the dosage of 0.05 g L−1 and KAl(SO4)2 with the dosage of 0.04 g L−1 could be utilized to achieve the biomass recovery efficiency of 99.5% and 97.9%, respectively, within a duration of 5 min. An economic evaluation of the harvesting process showed KAl(SO4)2 to be the cheapest coagulant that could be feasibly used to recover algae at a large scale.

RESEARCH HIGHLIGHTS

• Harvesting efficiency of inorganic coagulants on native mixed algae was studied

• Iron and aluminium metallic salts showed the maximal flocculation efficiency

• FeCl3 (0.05 g l−1) showed a maximum of 99.56% biomass recovery in 5 min

• Sulphate salts of copper at higher dosage lessened flocculation efficiency

(5)

RESULTS AND DISCUSSION

The flocculation studies with the use of inorganic coagulants have been quite common in water treatment. However, to harness the native mixed microalgal consortia grown on specific media composition, algal-specific flocculation studies have to be explored. As the biomass recovery efficiency depends on the species-specific features of the microalgae, the flocculation potential of different inorganic metal salts were estimated in the present study. The results obtained in each case were also compared with the previous studies reported in literature. This study presents the rationale behind the variations in the flocculation efficiency of microalgal from the open ponds of the NIT Rourkela, which were enriched with diluted human urine using different inorganic metal salts in the subsequent subsections.

Algal characteristics and growth analysis

The microscopic image showed the presence of single large coccoid cells, smaller circular cells aggregated as clumps, colonial cells and filamentous-branched structures with cylindrical cells. The microalgal consortium isolated from the open ponds of the NIT Rourkela thus consisted of mainly Chlorella sp., along with Scenedesmus sp., Synechocystis sp. and Spirulina sp. (Figure 1(a)) as observed by microscopic examination at 100× magnification. Figure 1(b) shows the growth pattern of microalgal consortium in diluted urine. The specific growth rate of microalgae in urine media was found to be 0.26 per day with 6.5% (v/v) diluted urine media. The biomass productivity was found to be 211 mg L−1 per day with a biomass content of 2,520 mg L−1. Tuantet et al. (2014) reported the biomass content of 9,800 mg L−1 of Chlorella sorokiniana in a short path photobioreactor with 2–3 times diluted urine supplemented with Mg2+ ions. Similar studies have also been done by Chang et al. (2013) and Jaatinen et al. (2016) using Spirulina platensis and C. vulgaris, which showed a biomass content of 800 mg L−1 and 730 mg L−1, respectively using diluted urine as the nutrient media. A similar approach was followed while growing the mixed algal culture because the earlier reported studies also showed related algal species. The difference in the yield obtained in the present study and the cited literature might be due to the variations in the urine type, the nutrient content and other operational as well as environmental conditions. The biochemical and physiochemical properties of microalgae, the nutrient availability in urine and the acclimatization by microalgae for the nutrient sources is also responsible for the differences in the microalgal growth rate.

Figure 1

(a) Microscopic image of microalgal consortium from the open ponds of the NIT Rourkela and (b) growth curve of a microalgal consortium with diluted urine (6.5%) as a nutrient source.

Figure 1

(a) Microscopic image of microalgal consortium from the open ponds of the NIT Rourkela and (b) growth curve of a microalgal consortium with diluted urine (6.5%) as a nutrient source.

Flocculation efficiency of inorganic coagulants

Ferric chloride

Ferric chloride (FeCl3) showed the maximum efficiency of 99.5% at physiological pH 7.5–7.8 with 0.05 g L−1 concentration (Figure 2(a)). Udom et al. (2013) reported the highest efficiency for FeCl3 at 93% with a dosage of 122 mg L−1 at pH 6 for Chlorella zofingiensis. Chatsungnoen & Chisti (2016a) also reported that more than 95% of the microalgal biomass can be removed at the dosage of 250 mg L−1 FeCl3. It was found that with the increase in FeCl3 dosage from 12.5 mg L−1 to 62.5 mg L−1, the biomass removal efficiency increased from 62.5% to 99.5%, beyond which it decreased to 96%. The metallic salts of iron mostly use the mechanism of charge neutralization (Branyikova et al. 2018). The study by Wyatt et al. (2012) reported that the precipitates of ferric hydroxide (Fe(OH)3) are 10 times smaller than that of the microalgal cells. Most studies utilizing ferric ions reported higher harvesting efficiency due to the high surface charge density of these ions (Udom et al. 2013; Branyikova et al. 2018). The positively charged precipitate is attracted to the negatively charged microalgal cells, below the requisite dosage, and so the volume of precipitates formed might not be sufficient to flocculate the algal cells. Thus, an optimal concentration of FeCl3 is required to obtain the maximal flocculation.

Figure 2

Flocculation efficiency of harvesting microalgae: (a) FeCl3, (b) KAl(SO4)2, (c) Ca(OH)2, (d) FeSO4 and (e) CuSO4.

Figure 2

Flocculation efficiency of harvesting microalgae: (a) FeCl3, (b) KAl(SO4)2, (c) Ca(OH)2, (d) FeSO4 and (e) CuSO4.

Alum

Alum (KAl(SO4)2) is one of the most commonly used coagulants for flocculation studies. The flocculation efficiency of KAl(SO4)2 for harvesting the mixed algal consortium is shown in Figure 2(b). KAl(SO4)2 showed the maximum efficiency of 97.9% at the dosage of 0.04 g L−1 with pH 7.5–7.8. Similar to the above study, Loganathan et al. (2018) used 30 mg L−1 of KAl(SO4)2, resulting in 96% microalgal removal efficiency at pH 8.2. A slight decline in biomass removal efficiency was observed at 0.05 g L−1. Chen et al. (2013) reported 93% biomass removal efficiency with Scenedesmus sp., with an 0.3 g L−1 KAl(SO4)2 dosage. Biomass removal efficiency of 91% was reported for microalgae with 0.25 g L−1 KAl(SO4)2 (Koley et al. 2017). Ali et al. (2018) reported 91.6% maximal microalgal biomass removal efficiency with 0.2 g L−1 KAl(SO4)2 for Conocarpus erectus. The variation in pH and dosage, as well as the biomass removal efficiency, might be attributed to the microalgal species under consideration. Branyikova et al. (2018) reported that the concentration of aluminium salts required for charge neutralization depends on the size and surface characteristics of the algal cells. Similar to the ferric ions, aluminate ions also have a high surface charge density, which can be used to achieve significant microalgal recovery (Loganathan et al. 2018). Maintaining an optimal concentration of coagulant is essential to achieve the desired harvesting efficiency without unwanted contamination of the culture media.

Calcium hydroxide

Calcium hydroxide (Ca(OH)2) precipitates with the increase in pH that coagulates microalgal cells resulting in formation of stable agglomerates. Calcium ions with phosphate in the media often form calcium phosphate (Ca3(PO4)2) precipitates that have a positive surface charge, and are thus involved in the process of charge neutralization (Branyikova et al. 2018). For the current study, Ca(OH)2 concentration varied in the range of 0.075–0.25 g L−1 and the biomass removal efficiency is shown in Figure 2(c). It was found that at the dosage of 0.1 g L−1, a maximal flocculation efficiency of 45% was achieved. Chen et al. (2013) reported a 90% biomass harvesting efficiency with Scenedesmus sp. using 0.3 g L−1 Ca(OH)2. With a further increment in concentration, the microalgal biomass removal efficiency was found to decline gradually until 8%. The study by Vandamme et al. (2015) reported that significant calcium salt precipitation results in flocculation efficiency of 90% at a pH ranging from 10 to 10.5. Since the present study used a physiological pH much lower than 10, a lower flocculation efficiency was observed compared to the other cited literature.

Ferrous sulphate

Sulphate salts of iron are also expected to cause algal flocculation due to charge neutralisation. Maximal microalgal biomass removal efficiency of 65% was obtained with 0.3 g L−1 of FeSO4, as represented in Figure 2(d). The removal efficiency was found to increase with an increase in coagulant dosage. The dosage was restricted to 0.3 g L−1 because iron (metal) salts at higher dosage are often associated with corrosive effects (Branyikova et al. 2018). With the increase in coagulant dosage, the amount of Fe2+ available will be sufficient to cause charge neutralisation for achieving a significant biomass removal efficiency. Similar to the present study, Reyes & Labra (2016) reported a maximal microalgal biomass removal efficiency of 69% with 1.5 g L−1 FeSO4. A flocculation efficiency of 40% has been reported by Kwon et al. (2011) using sulphate salts of iron for separating Dunaliella tertiolecta. During water treatment, FeSO4 dosage usually varies between 5 and 50 mg L−1; however, the optimal dosage is dependent on the media conditions (Pal 2017). The study also reported that increasing the concentration of iron sulphate salts might result in unwanted corrosion at a real-time industrial scale, and thus would increase the maintenance costs. It is therefore not advisable to use a higher dosage of iron sulphates for microalgal biomass recovery.

Copper sulphate

The positively charged cations in CuSO4 could be used for reducing the repulsion between the negatively charged algal cells resulting in formation of flocs. It is evident from Figure 2(e) that as the dosage of CuSO4 increased, the microalgal biomass recovery was found to decline. Microalgal biomass removal efficiency of 52.4% was reported with 0.5 g L−1 of CuSO4. With a further increase in the dosage to 2 g L−1, the algal harvesting efficiency declined to 33.3%. Following a gradual increase in dosage, no significant biomass removal efficiency was observed. Flocculation efficiency depends on the coagulant dosage as well as the algal cell abundance (Udom et al. 2013). The concentration 0.25 and 0.3 g L−1 of CuSO4 did not show any flocculation because a higher dosage resulted in contaminating the solution and thus resulting in the loss of algal biomass.

Similar to the above study, Rial et al. (2015) reported the microalgal biomass removal efficiency of nearly 60% with 0.5 g L−1 CuSO4, with no significant change in harvesting efficiency with a further increase in coagulant dosage. In contrast to the present study, Vera Morales et al. (2016) reported the flocculation efficiency of CuSO4 to be less than the alkaline agent Ca(OH)2. Studies by Rial et al. (2015); Vera Morales et al. (2016) and Kansole & Lin (2017) reported that using a higher dosage of CuSO4 can have toxic effects and result in residual deposition of ions over the algal biomass, thereby increasing the downstream processing costs. It was also observed in the present study that with the increase in concentration of CuSO4, the supernatant solution after flocculation was found to be blue in colour. The colour retained by the culture media is expected to hinder the reuse/recycle of the culture medium. Hence, the use of a high concentration of CuSO4 during biomass harvesting is limited.

Comparative efficiency of different flocculants in terms of flocculation time-period

The efficiency of different inorganic coagulants in terms of the dosage, biomass recovery efficiency and flocculation time (minimum time to achieve the highest efficiency beyond which it remained constant for 1 h) is shown in Table 1. Among all the inorganic coagulants it was found that FeCl3 (0.05 g L−1) showed the maximal biomass removal efficiency within 5 min, beyond which it remained constant over a period of 1 h. KAl(SO4)2 at a dosage of 0.04 g L−1 showed an algal harvesting efficiency of 97.9% within 5 min. For Ca(OH)2, the dosage of 0.1 g L−1 resulted in maximal removal efficiency of 45% after 20 min. Inorganic salts of FeSO4 and CuSO4 with a dosage of 0.3 g L−1 and 0.5 g L−1 showed the maximal harvesting efficiency of 65% and 52.4% within the flocculation time of 20 min and 30 min, respectively.

Table 1

Comparison of flocculation efficiency of different inorganic coagulants

CoagulantCoagulant dosage (g L−1)Flocculation time (min)Max. removal efficiency (%)
Ferric chloride (FeCl30.05 99.5
Alum (KAl(SO4)20.04 97.9
Calcium hydroxide (Ca(OH)20.10 20 45.0
Ferrous sulphate (FeSO40.30 30 65.0
Copper sulphate (CuSO40.50 20 52.4
CoagulantCoagulant dosage (g L−1)Flocculation time (min)Max. removal efficiency (%)
Ferric chloride (FeCl30.05 99.5
Alum (KAl(SO4)20.04 97.9
Calcium hydroxide (Ca(OH)20.10 20 45.0
Ferrous sulphate (FeSO40.30 30 65.0
Copper sulphate (CuSO40.50 20 52.4

Different researchers, including Chen et al. (2013), Vandamme et al. (2015) and Chatsungnoen & Chisti (2016a) have used several multivalent metal cations for flocculating algal biomass. The trend of flocculation for FeCl3 and KAl(SO4)2 in the present study was found to be similar to the study reported by Reyes & Labra (2016). The algal harvesting efficiency was almost constant after the dosage of 0.02 g L−1 and 0.0375 g L−1 for KAl(SO4)2 and FeCl3, respectively. Both Al3+ and Fe3+ in H2O are hydrated to a certain extent and have a hydration shell with six octahedrally coordinated water molecules. The soluble aluminate and ferric metal ion species play an important role during the coagulation process (Reyes & Labra 2016). Aluminium and iron salts provide cationic hydrolysis products that adsorb onto the microalgal cells causing charge neutralization (Chen et al. 2013). Both the metal ions have high surface charge density compared to other metallic salts. The solubility of ferric ions is higher at a broader range of pH, compared to aluminate ions that work at pH 6. Lower concentration of Al3+ ions could therefore precipitate with hydroxyl ions and achieve a higher flocculation efficiency compared to ferric ions. Destabilization depends on the algal concentration and their electrophoretic mobility, and thus an optimal concentration of positively charged hydrolysing ions is necessary to cause charge neutralization by adsorption onto the surface of negatively charged algal cells. Both the inorganic coagulants produce trivalent metal ions with high surface charge density, and the cell-to-cell collisions in the suspension therefore increases and hence the combination of these coagulants is expected to improve the flocculation efficiency (Loganathan et al. 2018).

Equilibrium is often achieved after an optimal dose; hence, there is no further significant increase in flocculation efficiency beyond it (Branyikova et al. 2018). The efficiency of flocculation and the flocculation time depends on the characteristic features of the coagulant along with the biomass to be harvested. The efficiency reported for FeCl3 is comparable to that of the removal efficiency of over 90% as reported studies by Wyatt et al. (2012) and Chatsungnoen & Chisti (2016a). It has also been reported that at the media pH ranging from 7 to 8, the positively charged Fe(OH)3 precipitates and monomeric hydroxy and ferric cations dominate, which often results in significant charge neutralization. KAl(SO4)2 has also proven to be an efficient coagulant for different microalgal cultures, in different dosages ranging from 50 to 300 mg L−1. With Scenedesmus sp., Chen et al. (2013) reported flocculation efficiencies of 97.3%, 94.9% and 90% with FeCl3 after 2 min, KAl(SO4)2 over 10 min and Ca(OH)2 after 120 min, respectively. Rial et al. (2015) reported the maximal biomass efficiency was achieved with 200 mg L−1 of metal salts after 510 min for Chaetoceros gracilis. Due to the difference in surface charge density of microalgal cells, there is a variation in requisite concentration of inorganic coagulant to achieve the desired flocculation efficiencies at the appropriate flocculation time.

Evaluation of economics of algal harvesting using inorganic salts

Algal harvesting occupies 20–30% of the total process costs (Vandamme et al. 2015); therefore, it is essential to analyse the costs of using these inorganic coagulants for recovering algal biomass (Table 2). It could be concluded that among all the inorganic coagulants, KAl(SO4)2 is the cheapest (0.014 US$per m3 of algal culture broth). Fecl3 with 99.5% flocculation efficiency (highest) incurs harvesting costs of 0.022 US$ per m3. The costs associated depends on the dosage of the coagulant used as well as the flocculation efficiency (Rial et al. 2015). Inorganic coagulants like KAl(SO4)2 could be used efficiently for harvesting algal biomass at a large scale. The low dosage with higher efficiency is expected to be commercially affordable with relatively lesser contamination issues for processing the algal biomass into biofuel.

Table 2

Harvesting costs in dollar ($) per m3 of algal culture broth Inorganic coagulantPrice of coagulant (US$ per gram)Process cost (US$per m3) Ferric chloride (FeCl34.48 × 10−4 0.022 Alum (KAl(SO4)23.36 × 10−4 0.014 Calcium hydroxide (Ca(OH)21.26 × 10−4 0.028 Ferrous sulphate (FeSO41.40 × 10−4 0.065 Copper sulphate (CuSO42.59 × 10−3 2.471 Inorganic coagulantPrice of coagulant (US$ per gram)Process cost (US\$ per m3)
Ferric chloride (FeCl34.48 × 10−4 0.022
Alum (KAl(SO4)23.36 × 10−4 0.014
Calcium hydroxide (Ca(OH)21.26 × 10−4 0.028
Ferrous sulphate (FeSO41.40 × 10−4 0.065
Copper sulphate (CuSO42.59 × 10−3 2.471

The residual deposition of flocculants over the algal biomass influences the yield of products, and their subsequent downstream processing and overall cost economics. Borges et al. (2011) reported that the anionic flocculants increase the saturated fatty acid content of microalgae. Cationic flocculants, on the other hand, increased the extractability of unsaturated fatty acids. Rwehumbiza et al. (2012) reported that the use of KAl(SO4)2 during flocculation did not interfere with the quality of fatty acid methyl esters and the residual aluminium levels were found to be very low. Use of alkaline coagulants like NaOH increased the concentration of saturated fatty acids and decreased the levels of polyunsaturated C20:4 and C20:5 fatty acids (Borges et al. 2016). Borges et al. (2011) reported that the residual flocculants on the algal surface form inter-bridges and loops, thereby helping trap special complex lipids by weak London forces, which influences the fatty acid profile. The utilization of cationic and alkaline flocculants also reduces the content of polyunsaturated fatty acids, thereby producing biodiesel with better oxidative stability (Borges et al. 2016). Chatsungnoen & Chisti (2016b) reported that the residual flocculants over the biomass did not influence the recovery of total lipids during solvent extraction irrespective of the algal species used. As the present study was carried out to process the biomass for biofuel, the use of KAl(SO4)2 might prove to be advantageous in terms of the biomass recovery efficiency, as well as the quality and quantity of product to be derived, without incrementing the associated costs.

CONCLUSION

The dosage of flocculants and the resultant biomass recovery efficiency depends on the species-specific features of the microalgae. The present study evaluated the flocculation efficiency of FeCl3, KAl(SO4)2, Ca(OH)2, FeSO4 and CuSO4 for harvesting a native microalgal consortium enriched with diluted human urine. Fecl3 and KAl(SO4)2 showed maximal flocculation efficiency. The study found that 0.05 g L−1 FeCl3 over a flocculation time of 5 min resulted in a biomass harvesting efficiency of 99.5% at the physiological pH with an algal concentration of 0.5 g L−1, and 0.04 g L−1 of KAl(SO4)2 showed harvesting efficiency of 97.9% within 5 min. Other metal salts could reach a maximum (45–65%) of biomass removal efficiency with a higher flocculation time. Estimation of the harvesting costs showed KAl(SO4)2 to be commercially feasible for harvesting the algal consortium at a large scale. Such studies are essential for identifying the requisite coagulant and the subsequent dosage with appropriate flocculation time for achieving the maximum biomass recovery without altering the physicochemical parameters of the microalgal culture at low cost and less time.

ACKNOWLEDGEMENT

The authors thank the Department of Biotechnology and Medical Engineering of the NIT Rourkela for providing the necessary research facilities. The authors thank the Ministry of Human Resources and Development of the Government of India (GoI) for providing the PhD fellowship to the first author. The authors acknowledge the Ministry of External Affairs of the GoI for sponsoring the grant under ASEAN-India Collaborative Research & Development scheme (CRD/2018/000082).

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