Microalgal harvesting using foam flotation: A critical review

Biomass and Bioenergy 120 (2019) 176–188

Contents lists available at ScienceDirect

Biomass and Bioenergy journal homepage: www.elsevier.com/locate/biombioe

Review

Microalgal harvesting using foam flotation: A critical review Haiyang Zhang

a,b

, Xuezhi Zhang

T

b,c,∗

a

Key Laboratory of Solid Waste Treatment and Resource Recycle Ministry of Education, Southwest University of Science and Technology, Mianyang, Sichuan, 621010, China b Center for Microalgal Biotechnology and Biofuels, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, Hubei, 430072, China c Key Laboratory for Algal Biology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, 430072, China

A R T I C LE I N FO

A B S T R A C T

Keywords: Microalgae Harvesting Foam flotation Bubble Biofuel

Microalgae are a promising feedstock for renewable biofuel to replace traditional fossil energy. However, one of the major challenges of the commercialization of microalgal biofuels is the efficient and economical harvest of microalgal biomass. Foam flotation, a high-efficiency separation technique originating from the mineral industry, has been adopted recently for potential application in harvesting microalgal biomass. This work critically reviews the principles and current status of microalgal harvesting using foam flotation by summarizing the advantages and challenges as well as the influence of biotic and abiotic factors, analyzing the economic feasibility, and proposing some new techniques as well as future research needs, using an illustrative process flow diagram. This work expands our understanding of microalgal harvesting using foam flotation, which may expedite the research and application of foam flotation in the downstream processing of microalgal biomass for the production of biofuel and bioproducts.

1. Introduction With the increasing shortage of fossil energy and rising environmental pollution, the search for environmentally friendly and renewable bioenergy feedstock has received extensive attention for the reconstruction of our energy structure [1]. Microalgae are considered ideal energy crops because of their numerous notable advantages, such as a short growth period, high lipid content, and no requirement for arable land [2,3]. They also have the potential for the coproduction of nutraceuticals, foods and other value-added products [4]. Meanwhile, microalgae present higher CO2 capture capacity by photosynthesis than land-based crops, which can reduce the emission of greenhouse gasses into the atmosphere [5]. In recent years, various studies have been carried out on microalgae-based biofuels, mainly including algal species selection and development, mass cultivation, harvesting and dewatering, and lipid extraction and conversion [6]. However, biofuels from microalgal biomass are still not commercially viable because these processes remain more expensive than conventional fossil fuels [7]. One of the major challenges for the commercial-scale production of biofuel from microalgae is to exploit an efficient and economical method of harvesting microalgae from dilute liquid suspensions [8]. Generally, the harvesting step accounts for 20–30% of the total biomass production costs [9], largely due to the small cell size (1–30 μm), similar density to ∗

water and low concentration (0.1–5 g L−1) [10]. As yet, none of the microalgal harvesting methods have proven economically viable and efficient for large-scale biofuel production [11]. Some commonly used separation approaches including sedimentation, filtration, centrifugation, and flotation have been adopted for harvesting microalgae [12]. Centrifugation is a rapid and efficient harvesting method [11]. However, it is generally preferred for high value-added algal biomass recovery due to its high energy consumption (approximately 8 kWh m−3) [13]. Gravity sedimentation is an effective and low-cost solid-liquid separation method for high-density materials. However, it is not suitable for harvesting microalgae due to its low loading rate [14]. Membrane filtration provides high quality biomass free of chemical contamination, along with recyclable water [15], especially for smaller single-cell species [16]. Nevertheless, due to membrane fouling, large-scale harvesting using membrane filtration is still challenging. Currently, flotation is widely employed for the solid-liquid separation of micron and submicron particles due to its high area loading rate, relatively short separation times, and most importantly, low device costs [17]. It has been applied to remove microalgae in the water treatment industry at a commercial scale [18]. Foam flotation, one of several flotation technologies, features a low cost of bubble generation and high particle-bubble adhesion efficiency and has been widely used in the mineral industry [19]. In recent years, foam flotation has been

Corresponding author. Center for Microalgal Biotechnology and Biofuels, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, Hubei, 430072, China. E-mail address: [email protected] (X. Zhang).

https://doi.org/10.1016/j.biombioe.2018.11.018 Received 17 April 2018; Received in revised form 14 October 2018; Accepted 16 November 2018 0961-9534/ © 2018 Elsevier Ltd. All rights reserved.

Biomass and Bioenergy 120 (2019) 176–188

H. Zhang, X. Zhang

Abbreviations DAF DiAF EF OD CTAB

DAH DPC DN2 PZC SDS AOM

Dissolved air flotation Dispersed air flotation Electro-flotation Optical density Cetyl trimethylammonium bromide

Dodecyl ammonium hydrochloride Dodecyl pyridinium chloride N-dodecylpropane-1,3-diamine hydrochloride Point of zero charge Sodium dodecylsulfate Algogenic organic matter

is generated between the cell and bubble, which causes the cell to adhere to the bubble. Consequently, the resistance of the liquid film must be conquered before a particle attaches to a bubble, and this process depends mainly on the surface physical and chemical properties of the particle [26]. Research has shown that a particle with a hydrophobic surface is more likely to attach to a bubble than a particle with a hydrophilic surface [27]. Therefore, foam flotation usually aims to add chemical collectors to increase the hydrophobicity of the particle and thus increase the floatability of particles. In microalgal foam flotation, harvesting/separation efficiency (HE) is commonly employed to indicate the harvesting performance [20,28–30] and can be calculated by the following equation:

tested for the harvest of microalgal biomass from dilute liquid suspension [20]. This method has demonstrated high potential for microalgal harvesting because of its high efficiency (> 90%) and low energy consumption (∼0.075 kWh kg−1 DW) [21]. This study aims to critically review the recent advances in microalgal harvesting using foam flotation by discussing the influences of biotic and abiotic factors, analyzing economic feasibility, introducing constraints relevant to large-scale application, and proposing future research needs using an illustrative process flow diagram. This review provides some useful information on the development of economical and efficient microalgal harvesting technology using foam flotation, which is expected to accelerate the commercialization of microalgaebased biofuel and bioproducts.

HE = (1 − CA/ CB ) × 100% 2. Microalgal harvesting using foam flotation: principles, advantages, and recent advances

(1)

where CA and CB are the concentration of microalgal cells after and before harvesting, respectively. Generally, the concentration of microalgal cells can be measured by the number (cell mL−1) or dry weight (g L−1) of microalgal cells per unit volume as well as by the optical density (OD) at certain wavelengths (e.g., 750 nm) using a spectrophotometer. However, the harvesting/recovery efficiency gives no assessment of the enrichment capability of foam flotation, which is a significant parameter for subsequent dewatering and drying. Therefore, most studies on microalgal harvesting have adopted the harvesting/recovery efficiency and enrichment ratio/concentration factor (ER/CF) simultaneously, and the enrichment ratio or concentration factor can be determined by equation (2).

2.1. Principles of foam flotation Flotation is an effective separation technique, originating from the mineral industry and subsequently widely applied in chemical engineering as well as water and waste water treatment. With the extension of its application, flotation can be divided into dissolved air flotation (DAF), dispersed air flotation (DiAF), electro flotation (EF) and other flotation [22]. Foam flotation, or froth flotation, is a type of DiAF. It functions based on the surface physical and chemical properties of particles. Briefly, particles are captured by bubbles with the help of collectors and rise with the bubbles to the surface of the aqueous solution (Fig. 1), achieving solid-liquid separation [17]. Foam flotation can usually be divided into three major steps [18]: (I) bubble generation; (II) collision and adhesion between particles and bubbles under the influence of a collector; and (III) steady foam layer generation, carrying particles to the top of the flotation device. The collision and adhesion phases play a significant role in foam flotation, directly influencing flotation performance [23]. In the collision and adhesion phases of foam flotation, particles and bubbles are close to each other, driven by hydrodynamics, as illustrated in Fig. 2 using microalgal cells as an example. When the cell encounters a rising bubble and traverses the different zones around the bubble [24], the liquid films around the cells and bubbles are compressed, thinned and ruptured, and the cell becomes attached to the bubble. In the outermost zone (zone 1, main flow zone), the interaction between the cell and bubble is the only hydrodynamic interaction that disturbs the cell close to the bubble. The intermediate region, named the shear zone (zone 2), is an asymmetric region where the adsorbed ions mainly gather under the bubble due to the tangential flow formed by the rising bubble. The inertial force and electrostatic repulsive force dominate the interaction. Therefore, collision between cells and bubbles occurs mainly in these two zones (zone 1 and zone 2). The innermost region, the adhesion zone (zone 3), is where interactions are actuated by the surface forces, including repulsive van der Waals, electrical double layer forces and attractive hydrophobic forces. These three zones overlap without obvious boundaries [25]. When the cell is close to the bubble, the thickness of the liquid is compressed to hundreds of nanometers until rupture; subsequently, a steady wetting area

(2)

ER = CF / CI

where CF is the concentration of microalgal cells in the harvested

Fig. 1. Microalgal harvesting using foam flotation. 177

Biomass and Bioenergy 120 (2019) 176–188

H. Zhang, X. Zhang

flotation, and the differences affect bubble size and energy consumption. In DAF, first, air is dissolved in water under high pressure (≥0.5 MPa) by an air compressor or a DAF pump, forming water saturated with dissolved air. Subsequently, gas molecules are released by the rapid dissipation of air-saturated water, and a mass of microbubbles with an average diameter of 50–60 μm are generated through coalescence between many small bubbles (gas nucleus) [32]. In foam flotation the bubbles can be generated from air dispersed by a microporous sparger, mechanical agitator or special bubble generator [33], and the size of the bubbles can range from 10 to 3000 μm in diameter [17]. Generally, the generation of bubbles in foam flotation is more energy efficient than the generation of bubbles by dissolved air under high pressure in DAF [17]. Different flotation reagents are used in DAF and foam flotation, including coagulants for DAF and collectors for foam flotation, which further determine the interactions between microalgal cells and bubbles. Generally, microalgal cells are difficult to directly adhere to microbubbles, mainly due to the same electronegativity and inverse polarity between the microalgal cell and the microbubble [34]. Therefore, harvesting microalgae by DAF is usually assisted by precoagulation/ flocculation, achieved by adding a high valence metal salt (Al3+, Fe3+) or polymeric coagulant (polyacrylamides, polyaluminum chloride) [31]. Microalgal cells are aggregated for floc generation, which can be attached to bubbles by the interception effect and electrostatic interaction [35]. However, in foam flotation, it is generally recognized that the hydrophobicity of microalgal cells is improved by the addition of collectors/surfactants (e.g., cetyl trimethylammonium bromide, abbreviated as CTAB), and the attachment of bubbles to microalgal cells is driven mainly by hydrophobic interactions that are stronger than the interception effect or electrostatic interaction [36]. The bubble coalescence is obstructed by the surfactant due to the decreasing interface surface tension, which stabilizes the foam, resulting in a higher concentration factor than in DAF for the prolonged drainage through the channel walls of the foam, especially in a foam flotation column [21]. Additionally, foam flotation has been proven to process greater volumes of microalgae more quickly and with less energy than DAF [37]. In conclusion, foam flotation has advantages over DAF in lower energy consumption of bubble generation, attachment stability of microalgal cells to bubbles, improved concentration factor and higher loading rate.

Fig. 2. Zones of interaction between a bubble and a particle.

product, and CI is the initial concentration of microalgal cells. A new equation (3) can be obtained by substituting the volume of microalgal suspension before (VB) and after (VA) foam flotation, and the volume of foam product (VF) into equations (1) and (2). According to equation (3), the enrichment ratio exhibits a relationship with the harvesting efficiency and volume of the foam product.

ER = 1 + HE × (VB − VF )/ VF

(3)

2.2. Advantages of foam flotation over dissolved air flotation Dissolved air flotation (DAF) is an efficient solid-liquid separation method that is initially applied in water treatment [18]. Recently, it has received extensive attention for application in microalgal harvesting [31]. There are notable differences between DAF and foam flotation, mainly reflecting the nature of bubble generation, flotation reagents and the interaction between microalgal cells and bubbles. Bubble generation is completely different in DAF and foam Table 1 Main research on microalgal harvesting using foam flotation. Microalgal species

Microalgal concentration

Collector type

Collector concentration

pH

Harvesting efficiency

Concentration factor

Reference

Chlorella sp. (High temperature strain) Chlorella vulgaris

–

Spontaneous froth without flotant Sodium oleate

–

3.0

88%

–

3.0

75.20%

–

40 mg L 20 mg L−1 + 10 mg L−1 40 mg L−1 20 mg L−1 + 10 mg L−1 100 mg L−1 100 mg L−1 3 mg L−1 80 mg L−1 10 mg L−1

8.0 ± 0.1 8.0 ± 0.1 4.0–7.0 7.0–8.0 7.8 3.5 9.5

> 90% > 90% > 90% > 90% 90% 80% 99% 80% –

–

Levin et al., 1962 Philip et al., 1968 Chen et al., 1998

–

Liu et al., 1999

–

Phoochinda et al., 2003 Garg et al., 2012

25 mg L−1 60 mg L−1 20 mg L−1 + 5 mg L−1 60 mg L−1 20 mg L−1 + 10 mg L−1 25 mg L−1 15 mg L−1 50 mg L−1

6.0 6.89 ± 0.4

97.4% > 93.7% ∼94% > 93.7% ∼98% 93.2% 99% 90.1% 94.5%

11.4 –

– 4

−1

Scenedesmus quadricauda Chlorella sp.

7.4 × 10 cells ml

Scenedesmus quadricauda Chlorella sp. BR2 Tetraselmis sp. M8 Chlorella sp.

1 × 105 cells ml−1

CTAB SDS + chitosan CTAB SDS + chitosan CTAB SDS

–

C14TAB

0.11 ± 0.08 g L−1

CTAB

Tetraselmis sp. M8 Chlorella vulgaris

– 1.48 ± 0.2 (OD)

Scenedesmus obliquus

2.6 ± 0.2 (OD)

Tetraselmis sp. M8

–

DAH CTAB Saponin + chitosan CTAB Saponin + chitosan DN2 DPC

Chlorella vulgaris Anabaena vasriabilis

–

CTAB

–

−1

1.5 mg L

−1

178

–

7.77 ± 0.05 6.0 9.5 10.0

– 230

Coward et al., 2013 Garg et al., 2014 Kurniawati et al., 2014

– 11 23 ∼3.1–10.2

Garg et al., 2015 Wen et al., 2017

Biomass and Bioenergy 120 (2019) 176–188

H. Zhang, X. Zhang

foam flotation. The effects of the properties of microalgal cells on flotation performance are discussed below.

Foam flotation has been widely applied in mineral separation at the industrial scale and has been adopted to achieve the efficient and economical harvesting of most marine and freshwater microalgae in the laboratory. Mineral particles and microalgal cells share many similarities, such as fine size, low concentration, and negatively charged and polar surfaces. Therefore, foam flotation may have the greatest potential among microalgal harvesting methods due to its high harvesting efficiency, low energy consumption, simple operation, few additional accessories and low space required for installation.

3.1.1. Cellular morphology Microalgae species vary in morphology (shape and size) [41]. For example, Microcystis sp. and Chlorella sp. are spherical cells with a size of 2–6 μm, the shape of Chlamydomonas angulosa is oval with a diameter of 6–12 μm, and Phormidium sp. and Melosira sp. have filamentous shapes with an average length of ∼20 μm. The flotation efficiencies of different microalgal species are also obviously impacted by the morphologies [29]. Bui et al. [42] investigated the effect of cell shapes (spherical, oval and filamentous cells) on microalgal removal efficiency using microbubble flotation and noted that the number of removed cells was in the order of filamentous > oval > spherical algae, which may be due to the longer/more contact perimeter/points between the bubble and filamentous microalgal cell than those between the bubble and oval/spherical microalgal cell. The influence of the shape and size of mineral particles on the flotation performance has been well studied, which might provide some insights for future studies on the influence of microalgal morphologies. The shape of mineral particles has been proven to play a significant role in collision and attachment during flotation [43]. Xia et al. [44] reported that irregular, elongated and flattened particles attach easily to bubbles, whereas spherical particles are easily detached from bubbles. The edges of the shape are directly related to the film rupture, which influences the attachment time. A shorter attachment time is required for an irregularly shaped particle to be captured by a bubble than for a spherical particle. Meanwhile, the elongated particle provides a large contact line and area for particle-bubble attachment, making it difficult to detach from the bubble. In conclusion, the effect of cell shape on microalgal foam flotation is mainly dominated by the attachment stability between the microalgal cell and bubble, which may be determined by the length of the contact perimeter and the number of contact points (Fig. 3). Particle size is another very important factor influencing flotation performance [45]. According to the model of theoretical collision and attachment [46], if the other conditions are kept constant, the collision efficiency increases but the attachment efficiency decreases with increasing particle size. However, the optimum particle size distributions for most minerals are in the range of approximately 20–100 μm [47].

2.3. Recent advances in microalgal harvesting using foam flotation Foam flotation was highlighted as a potential method for harvesting microalgal biomass in 1962 [38]. Unfortunately, foam flotation has not received sustained attention until recent years, with the new regard for microalgae as an ideal feedstock for biofuel and bioproducts. The recent studies on microalgal harvesting using foam flotation are summarized in Table 1. Foam flotation can be appropriate to harvest various microalgal species, including single-celled freshwater species (Chlorella, Scenedesmus, and filamentous freshwater strain Anabaena) as well as marine species (Tetraselmis), for a wide range of initial concentrations. A high harvesting efficiency of more than 90%, with a concentration factor reaching 230 was achieved with the assistance of cationic collectors, including cetyl trimethylammonium bromide (CTAB), dodecyl ammonium hydrochloride (DAH), dodecyl pyridinium chloride (DPC) and N-dodecylpropane-1,3-diamine hydrochloride (DN2), or with combined reagents including a cationic coagulant and anionic collectors at concentrations below 20 mg L−1. The results demonstrated that foam flotation is a highly efficient method for microalgal harvesting. Garg et al. studied the harvest of marine microalgae (Tetraselmis sp. M8) using foam flotation with the assistance of CTAB and found that microalgal hydrophobicity played a crucial role in determining the flotation performance [20]. Coward et al. [21] carried out a series of fractional factorial experiments to determine the relative importance of key design and operational variables (air flow rate, batch run time, foam column height, surfactant concentration, and surfactant type) in foam flotation for microalgal harvesting. Under optimized conditions, the harvesting efficiency could reach up to 90%, and it consumed only 0.075 kWh kg−1 DW. The harvesting efficiencies of foam flotation assisted with cationic surfactants are higher than those with anionic surfactants [39]. The bubble size also plays a decisive role in the harvesting efficiency of foam flotation, and smaller bubbles can enhance the collision and attachment between bubble and microalgal cells, resulting in significantly faster rise velocities than larger bubbles [40].

3.1.2. Hydrophobicity The hydrophobicity of a particle plays a key role in determining its floatability, as it determines the particle-bubble attachment in foam flotation [48]. Hydrophobic interaction is an attractive force for the attachment of particles to bubbles, whereas van der Waals and electrostatic forces are repulsive for the majority of conditions [23]. Ducker et al. [49] found that the hydrophobicity of particles was directly

3. Biotic and abiotic factors influencing microalgal harvesting using foam flotation Foam flotation is a physical and chemical separation method that functions via the three interfacial interactions among microalgal cells, bubbles and culture media. In principle, the factors affecting the properties of the three interfaces will influence the efficiency of foam flotation, mainly including the biotic of the microalgal cells (cellular morphology, hydrophobicity, zeta potential, surface functional groups, and presence of algogenic organic matter-AOM), and abiotic factors such as collector/surfactant type and concentration, properties of the bubbles (size, zeta potential and stability), media chemistry (pH, ionic strength, alkalinity) and operating parameters (flotation time and air flow rate). 3.1. Properties of microalgal cells The direct capture of microalgal cells by bubbles is difficult due to the small size of the cells, the negative charge on their surface as on the bubble, and their strong hydrophilicity. Therefore, changing the surface properties of microalgal cells is required for efficient harvesting using

Fig. 3. The influence of microalgal cell shape on the cell-bubble attachment. 179

Biomass and Bioenergy 120 (2019) 176–188

H. Zhang, X. Zhang

Therefore, the surface functional groups are a significant factor for harvesting microalgae by foam flotation because of their influence on zeta potential and hydrophobicity. Zhang et al. [61] demonstrated that the flotation performance of Chlorella zofingiensis exhibited a linear relationship with the Al3+ dosage and concentrations of surface functional groups. Wen et al. [29] reported that Anabaena variabilis exhibited a higher flotation performance than Chlorella vulgaris, which was mainly attributed to the larger number of hydrophobic groups, such as C52+XH98+2XO (X = 0–12), CXH2X−2O (X = 15, 17, 19) and CXH2X−10O (X = 32, 33, 34), carried on the cell wall of A. variabilis.

correlated with the attractive force between particles and bubbles. However, most microalgal species are naturally hydrophilic [50]. Therefore, harvesting microalgal biomass by foam flotation usually requires adding a collector/surfactant to increase the hydrophobicity of the cell [21]. Garg et al. [30] found that the hydrophobicity of microalgal cells could be enhanced by increasing the dosage of DAH, and foam flotation assisted with cationic surfactants was an advantageous method for microalgal harvesting, especially with the low surface hydrophobicity of marine microalgae (Tetraselmis sp. M8). Additionally, they indicated that the hydrophobicity of the cell exhibited a positive linear relation with the harvesting efficiency [51].

3.1.5. Microalgal growth conditions Different microalgal bioproducts are produced by different microalgal species under specific culture conditions. For example, proteins are produced in the exponential growth phase, while lipids and antioxidant pigments are often produced in the stationary phase under the stress of high light and nutrient starvation [7,62]. The growth conditions of microalgae determine the cellular surface characteristics and media properties [41,50,60]. Xia et al. [60] found that surface properties such as cell size, hydrophobicity, total concentration of functional groups and negative charge increased with culture age. Although the effects of growth conditions on the efficiency of microalgal harvesting using foam flotation have not been revealed, several studies have been conducted on the effect of growth conditions on the efficiency of DAF [61,63,64]. Zhang et al. [61] noted that the dosage of Al3+ required for the same flotation performance decreased when the microalgae were cultured from the exponential growth phase to the declining phase, although the concentration of AOM increased as the culture aged and consumed more Al3+. They also found that the Mg2+ dosage for harvesting microalgae by magnesium coagulation-flotation decreased as the growth phase extended, mainly due to the presence of large amounts of HPO42- and CO32- in the medium of the early exponential phase culture, which competed with the microalgal cells for Mg2+ [65]. Coward et al. [36] concluded that the concentration factor of foam flotation for microalgal harvesting was highest during the late exponential phase (12 days), which resulted from a reduction in the electrochemical stability of the cells during the other phases. The concentration of microalgal biomass is closely related to the culture conditions, generally ranging from 0.5 g L−1 to 5 g L−1 for autotrophic culture [66]. The initial concentration of particles was found influence other flotation conditions, such as collector dosage, flotation time and air flow rate [19]. Levin et al. [38] noted that with increasing feed concentration, the concentration factor of microalgal harvesting clearly decreased, and the effect of feed concentration on the concentration factor could be weakened by increasing the air flow rate.

3.1.3. Surface charge Microalgal cellular surface charge is another important characteristic for most separation methods and can be quantified using the polyelectrolyte titration method [52,53]. In practice, surface charge is usually indirectly indicated by the value of the zeta potential [54]. It has been confirmed that surface charge plays a significant role in microalgal flotation [29]. The zeta potentials of most microalgae strains are negative, ranging from −10 mV to −50 mV in natural culture solution [29,50]. When particles approach air bubbles, the electrical double layers surrounding the particles and bubbles overlap, causing a repulsive force due to the same negative charges carried on both surfaces, resulting in poor flotation performance [18]. Consequently, microalgae flotation is commonly combined with coagulation/surfactant or pH manipulation to invert the charges of the microalgal cells or bubbles. The surface charge of microalgal cells can also be used to determine the collector type (cationic or anionic) selection in microalgal foam flotation [39]. Phoochinda et al. [55] found that the recovery efficiency of Scenedesmus quadricau achieved by the addition of SDS (anionic surfactant) was less than 20%, whereas it was more than 90% with the addition of CTAB (cationic surfactant), mainly due to the negative charges carried on the microalgal cells. However, the harvesting efficiency could be improved to 80% by decreasing the pH to 3.5 because of the increase in electrostatic attraction between SDS and the positively charged microalgal cells (point of zero charge, PZC≈4). Moreover, Kurniawati et al. [56] noted that the zeta potential of microalgal cells was significantly changed by using CTAB as a flotation collector, which resulted in a high harvesting efficiency. Conversely, the small change in the zeta potential with the addition of saponin (anionic biosurfactant) resulted in poor flotation performance. Therefore, flotation performance can be evaluated by comparing the zeta potential changes of microalgal cells before and after the addition of a collector.

3.2. Collector type and concentration 3.1.4. Surface functional group The cell wall is the outermost shell of a microalgal cell and is composed of carbohydrate, protein and lipid components [57]. These substances contain different functional groups such as carboxyl, hydroxyl, amine, phosphoryl and other charged groups [58]. Research has shown [50,59] that the surface functional groups vary among different microalgal strains, resulting in diverse surface characteristics such as zeta potential and hydrophobicity. Garg et al. [41] reported that microalgae cells present a negatively charged surface mainly due to the abundant surface carboxyl, phosphoryl, and hydroxyl groups, and that the surface hydrophobic properties of microalgae were also affected by the structures of the cell wall and the surface groups. Hadjoudja et al. [59] found that the concentration of carboxyl groups on the surface of M. aeruginosa (1.60 × 10−3 mol g−1) was higher than that on C. vulgaris (0.22 × 10−3 mol g−1), resulting in a larger negative charge on M. aeruginosa. Similarly, Xia et al. [60] showed that the surface negative charge of oleaginous microalgae increased as the total concentration of functional groups increased.

In mineral foam flotation, a collector can be applied to improve the hydrophobicity of the target mineral because most minerals are hydrophilic [67]. The collector usually consists of a polar head and nonpolar tail. The hydrophilic polar head adheres to the surface of the mineral by electrostatic interaction or chemical reaction, which determines the adsorption strength and selection between the collector and mineral. Subsequently, the hydrophobic nonpolar tail is exposed in the solution to improve the hydrophobicity of the mineral. Similarly, most microalgae species are naturally hydrophilic, which hinders their capture by bubbles. According to their ionic properties. flotation collectors are generally divided into anionic, cationic, nonionic and amphoteric collectors [68]. The selection of collectors is commonly based on the adsorption mechanism of the collectors on the particles [69]. Generally, some surfactants, such as quaternary ammonium salts (CTAB, DAH, SDS, etc.) have been used for harvesting microalgae by foam flotation (Table 1). However, cationic surfactants are more effective than the other types of collectors in the natural cultural medium, mainly due to the dominant 180

Biomass and Bioenergy 120 (2019) 176–188

H. Zhang, X. Zhang

size. Similarly, Hassanzadeh et al. [74] selected various bubble sizes (0.08, 0.12 and 0.15 cm) to study the effect of bubble size on the collision efficiency experimentally and found that a small bubble with a low velocity resulted in a higher collision efficiency than a large bubble. Meanwhile, Yoon et al. [73] found that the attachment efficiency first presented an increasing trend with increasing bubble size until the bubble size reached 0.35 mm, after which continued increases in bubble size resulted in decreased attachment efficiency. Xing et al. [75] noted that the film drainage speed increased with decreasing bubble size due to the increased driving pressure, and when the bubble size was reduced from 3 mm to 1.5 mm, the equilibrium film thickness decreased from 172 nm to 98 nm, which resulted in a high attachment efficiency. Pan et al. [76] also found that the use of small bubbles was more effective for increasing the kinetics of film thinning and hence the flotation rate. Likewise, Coward et al. [40] reported that small bubbles could enhance the collision and attachment efficiencies and improve the flotation performance of microalgal harvesting. In conclusion, small bubbles are generally beneficial to promote collision between bubbles and particles. However, there may be an optimum bubble size range for achieving the highest attachment efficiency of bubble-particles, and the attachment efficiency will be decreased when the bubble size is larger or smaller than the optimum range. Consequently, the effect of bubble size on the collision and attachment efficiencies must be comprehensively considered to obtain optimal flotation performance.

electrostatic interaction between the collectors and the negatively charged microalgal cells [39]. Phoochinda et al. [55] studied the effect of surfactant type on the foam flotation performance of microalgae and found that CTAB resulted in a high efficiency up to 90%, whereas SDS led to a poor efficiency of 16%. However, Liu et al. [39] noted that the flotation performance assisted with SDS could be improved from 20% to more than 90% by the pre-addition of chitosan (10 mg L−1) due to the neutralization or reduction of microalgae surface charge. These results suggested that the adsorption of surfactant on the microalgal cell surface is crucial for hydrophobic surface modification, which favors cell-bubble attachment. The concentration of the collector is also a primary factor for the foam flotation of microalgae. Recent studies on the effects of collector concentration on the harvesting efficiency of microalgal foam flotation are presented in Fig. 4. Despite varying with microalgal species and cell concentration, media chemistry and the surface properties of the surfactant, the harvesting efficiency generally increased with increasing concentrations of different collectors, and then reached a plateau, as the collectors enhanced the hydrophobicity of the microalgal cells [20,29]. However, it was also reported that an overdose of collector reduced the enrichment factor [29,51,70]. According to the fitted curve in Fig. 4, the harvesting efficiencycollector dosage can be described using the following equation:

Harvesting Efficiency = −0.0235C 2 + 2.6852C + 12.798

(4)

where C is the concentration of the collector. Moreover, Guthrie et al. [65] reported that the hydrophobic capacity of the collector increased as the carbon chain length of the nonpolar tail increased, which resulted in an increase in flotation performance when recycling the diaspore and kaolinite. However, studies on the effect of carbon chain length of collectors on microalgal foam flotation have not yet been reported.

3.3.3. Zeta potential of bubbles It is well known that bubbles generally acquire surface charges in aqueous solutions due to the asymmetric dipoles of water molecules residing at the gas–liquid interface and the adsorption of ions [77]. Subsequently, an electric double layer forms around the bubble because of the effect of the surface charge of the bubble on the spatial distribution of ions in the solution, and this double layer plays an important role in bubble-particle attachment and bubble coalescence [77,78]. Zeta potential is also applied to determine the strength and polarity of the surface charges of bubbles, such as those on the particle. The zeta potential of the bubbles was reported to be negative, from 0 to −65 mV for a pH range of 2–12 in aqueous solution without the addition of chemical reagents [78], and the absolute value of the negative zeta potential increased with increasing pH [79]. Arturo et al. [80] found that positive charges were observed on the bubbles in solution with dodecylamine (25 ppm) as a cationic collector, and the zeta potential increased from +8 mV to + 25 mV as the pH decreased from 12 to 2. They also noted that the negative charge of bubbles could be enhanced by the addition of an anionic collector such as xanthate or

3.3. Bubble Bubbles are the carriers of particles and play a significant role in foam flotation for fine particle separation from dilute aqueous solution [25]. The capture of a particle by a bubble is the key step of flotation separation, which may be observably influenced by the characteristics of bubbles such as their size, shape, zeta potential and stability. 3.3.1. Bubble shape Guthrie et al. [71] reported that the shape of bubbles can be primarily classified as spheres, ellipsoids and spherical caps, which are mainly impacted by the size of the bubbles and the surface tension of the solution. Generally, smaller bubbles and lower surface tension of the solution result in a higher spherical degree [18]. Tsuge et al. [72] found that the trajectory of a bubble vibrated when the spherical degree was reduced, which would affect the attachment stability of the bubble and particle and the hydrodynamics of flotation. 3.3.2. Bubble size Bubble size is an important property in flotation and affects the efficiency of collision and attachment of particles to bubbles and the rise velocity of the bubbles [18]. According to the theoretical models of flotation [23], the capture efficiency E between a bubble and a particle may be defined as:

E = Ec × Ea × Es

(5)

where Ec is the collision efficiency, Ea is the attachment efficiency, and Es is the stability efficiency of a bubble-particle aggregate. Each of these efficiencies may be influenced by the bubble size and the particle size [73]. According to the equations derived by Ref. [73], the collision efficiency between bubbles and particles decreased with increasing bubble

Fig. 4. Effects of collector concentration on harvesting efficiency. 181

Biomass and Bioenergy 120 (2019) 176–188

H. Zhang, X. Zhang

electrostatic adsorption at a certain pH. For instance, an acylation reaction may take place between the carboxyl of the cell surface and the ammonium cationic collector. The pH of the solution can also affect the zeta potential and stability of the bubbles. Arturo et al. [80] reported that the zeta potential of air bubbles depended on pH and could be reversed at low pH or by the addition of a collector. Levin et al. [38] applied foam flotation to harvest high-temperature Chlorella and found that the stability of bubbles was inversely proportional to the pH, especially at pH values less than 4.5. They also noted that the concentration of harvested biomass decreased linearly with increasing pH. The adsorption of the collector on the microalgal cell surface is generally dominated by electrostatic forces [36], and consequently the adsorption quantity of the collector increased as the opposite potential difference increased. Therefore, the optimal pH of microalgal foam flotation may differ for different microalgal strains and collectors, largely due to the differences in the zeta potentials of cells and types of collectors. For instance, the cationic surfactant CTAB was found to be most effective at pH 7.8, whereas the optimal pH for the anionic surfactant SDS was 3.5 [55].

dithiophosphinate. Furthermore, the zeta potential of bubbles is impacted by the presence of metal ions in the solution. Han et al. [81] reported that the electronegativity decreased with increasing concentrations of Ca2+ or Mg2+; interestingly, charge reversal of bubbles (positively charged bubbles) was observed in solution with 10−2 M Mg, especially above pH 9. Therefore, opposite surface charges between bubbles and microalgal cells may be achieved by changing the solution conditions, such as by the addition of surfactants or metal salts, which would favor foam flotation harvesting. 3.3.4. Bubble stability Bubble stability is a property that describes the coalescence of bubbles and the foam carrying capacity, which affects the flotation performance [82]. According to the collision and attachment efficiency theory models [73], it is generally thought that small bubbles can enhance the collision and attachment efficiencies between bubbles and particles. The bubble coalescence can be restrained by reducing the surface tension of the aqueous solution to produce small bubbles, namely, increasing the stability of bubbles [83]. However, research found that increasing bubble stability would increase in the thickness of the liquid film between the colliding bubble and particle [84], which made it difficult to achieve bubble-particle attachment. Accordint to Subrahmanyam et al. [82], an excessively stable froth was difficult to handle, while an unstable froth was also less desirable. Therefore, the bubble stability must achieve a delicate balance of influences between the size of the bubbles and the thickness of the liquid film. In microalgal foam flotation harvesting, frequently-used surfactants such as CTAB, SDS and DAH can simultaneously improve the hydrophobicity of microalgal cells (as collectors), restrain the bubble-bubble coalescence and increase the bubble stability (as frothers). These effects can explain why the harvesting efficiency increases but the concentration factor decreases with increasing surfactant dosage.

3.4.2. Ionic strength Ionic strength influences the surface charge of a microalgal cell, the size, zeta potential and stability of a bubble, and the attachment efficiency between the microalgal cell and the bubble. According to the extended DLVO theory, increasing ionic strength can compress the electrical double layer, resulting in a decrease in the zeta potential of a microalgal cell [85] or bubble [77]. Chen et al. [86] found that the electrostatic interactions between a microalgal cell and collector would be weakened by increasing ionic strength; therefore, the flotation performance of microalgae at high ionic strength was poor. Yang et al. [77] noted that the negative zeta potential of bubbles decreased with increasing ionic strength at the same pH. Moreover, it was reported that at high ionic strength, bubbles were larger and tended to rupture more easily as they flowed upward to the foam layer, resulting in poor collecting performance for microalgae separation [39]. Ralston et al. [23] studied the effect of ionic strength on attachment efficiency by theoretical calculation and experimental verification and found that the attachment efficiency decreased with increasing ionic strength. Meanwhile, Pacheco et al. [87] reported that when the ionic strength increased, competitive adsorption might occur between metal ions and cationic collectors with negatively charged particles, decreasing the flotation performance.

3.4. Media chemistry Media chemistry describes the properties of the liquid phase, mainly pH, ionic strength and alkalinity. The effects of solution chemistry conditions on microalgal foam flotation are discussed below. 3.4.1. pH The pH of the solution is one of most important adjustable parameters for microalgal foam flotation, and plays an important role in the interfacial properties of the three phases, gas, solid and liquid, greatly affecting the flotation performance [29]. Research showed that the pH could influence the surface properties of microalgal cells, the zeta potential and stability of the bubbles, and the interaction mechanisms of collectors [29]. It is well known that some of the surface functional groups of microalgal cells, such as hydroxyl (-OH), amine (-NH2) and carboxyl (-COOH), are ionizable, that is, they can be protonated or deprotonated according to the pH of the solution [50]. For example, when the protonation of amine and carboxyl groups on the microalgal cell surface is dominant, i.e., at low pH, the residual surface charge is positive. In contrast, these surface groups are deprotonated at high pH, creating a negative surface charge. When the delicate balance between protonation and deprotonation is achieved, the residual surface charge is zero, which is called the point of zero charge (PZC). This behavior explains the pH dependent zeta potential of microalgae [85]. Furthermore, autoflocculation may be induced by the protonation of carboxylic acid on the microalgal cell surface at low pH (< 4), increasing the collision efficiency between aggregated cells and bubbles. The various types of microalgal surface groups are formed by protonation or deprotonation at different pH values, which may cause chemisorption between microalgal cells and collectors in addition to

3.5. Operational parameters In addition to the above main factors, such as the surface properties of microalgal cells, collectors, bubbles and solution chemistry, foam flotation is also influenced by operating parameters, such as flotation time, air flow rate and foam height. Chen et al. [86] found that the flotation performance increased with increasing flotation time in the initial phase, mainly due to the increased chances of bubble-cell collision. Subsequently, an approximate balance of flotation performance was reached as the flotation time was prolonged. However, the concentration factor decreased with overlong flotation time [30]. The air flow rate is also one of the operating parameters for foam flotation and may affect the bubble size, the collision chances of bubbles and particles and the hydrodynamic conditions of flotation [39]. However, when sufficient air bubbles are available for the cells, the air flow rate has little influence on flotation performance [86]. Foam height is also determined by the bubble stability and column height. As the foam height increases, the stay time of the foam is elongated, and the drainage is enhanced, which can improve the concentration factor. Levin et al. [38] reported that the concentration 182

Biomass and Bioenergy 120 (2019) 176–188

H. Zhang, X. Zhang

4.3. Jet foam flotation for microalgal harvesting

factor first increased rapidly and subsequently reached a plateau as the foam height increased from 5 to 110 cm.

Jet foam flotation has great potential for solid-solid, solid-liquid and liquid-liquid separation as well as in mineral processing, and it requires neither a mechanical agitator nor a compressed air system [17]. It mainly employs one or several bubble generators and pumps and a separation column (Fig. 7). Feed slurry is circularly pumped into the bubble generator, and a jet flow is formed due to the transformation of pressure energy into kinetic energy by the nozzle. Meanwhile, air is introduced into the suction chamber of the bubble generator and dispersed into bubbles by the jet flow [92]. The bubble formation processes in the bubble generator can be divided into three stages [93], as shown in Fig. 7. First, air is carried into the throat of the bubble generator by the viscous force of the liquid, and the relative movements of the gas, liquid and solid are formed due to their velocity differences. In this stage, both the gas and liquid are continuous phases, and the solid (microalgal cell) is a dispersive phase. The second stage mainly occurs in the throat of the bubble generator, where the liquid phase is sheared into droplets due to the higher amplitude induced by the intensity of the turbulent kinetic energy, whereas the gas phase is still continuous. In the third stage, the gas molecules obtain high kinetic energy under the action of droplets with high velocities, and the gas phase is crushed into microbubbles, while the droplets are regrouped into a continuous phase. The high-intensity turbulent energy formed by the jet flow can also promote the dispersion of flotation agents and the interaction of collector-particle. The collision and attachment of particles and bubbles occur subsequently in the extended pipe of the bubble generator and can be enhanced by a suitable velocity gradient [94]. Therefore, jet foam flotation can provide a stabilized flow field for the rising aggregations (bubble-particle) in the flotation column. Although the application of jet foam flotation for microalgal harvesting has not been reported, it may be the most potential foam flotation devices for harvesting microalgae, largely due to its high throughput, high efficiency, low energy consumption and moderate maintenance costs. Importantly, the intensity of the jet flow in the bubble generator must be appropriate to avoid microalgal cell damage, especially for fragile microalgal species (e.g. Dunaliella salina, Isochrysis galbana, Euglena gracilis, Arthrospira platensis).

4. Foam flotation devices for microalgal harvesting Various devices have been designed and implemented for the separation of different minerals. Generally, foam flotation can be classified into machine-stirred foam flotation, pneumatic foam flotation and jet foam flotation according to the different methods of bubble generation [88] that have been tested or have the potential to be applied in microalgal harvesting.

4.1. Machine-stirred foam flotation Machine-stirred foam flotation is mainly carried out by an impeller and a flotation tank (Fig. 5). Air is introduced into the negative pressure region formed by the high-speed stirring of an impeller, and subsequently, air is sheared into microbubbles under intense agitation. Meanwhile, the mechanical stirring action can improve the dispersion of flotation agents and the collision between bubbles and particles. Therefore, the impeller is a core component of machine-stirred foam flotation. Research has shown that the entrained-air volume is determined by the air dispersion capacity of the impeller and can be enhanced by increasing the blade number or impeller speed [88]. More small bubbles with thin liquid films will be generated under high agitation speed, and therefore, the collision and attachment efficiency will be increased [89]. However, extensive agitation also results in high energy consumption and high detachment, which affects the overall flotation performance [90]. In addition, the air self-induced method of machine-stirred foam flotation can be replaced by a compressed air driven pneumatic cell, resulting in high entrained-air volume, low rotation speed and energy consumption, stable interface interaction and little wear. Nevertheless, the pneumatic foam flotation machine needs an additional compressed air system and pipe, which increases the occupied space and the capital investment and maintenance cost. Machine-stirred foam flotation was first adopted to harvest microalgae (Chlorella vulgaris) by Smith et al. [33] in 1968. Wen et al. [29] used a laboratory-scale Denver flotation cell to harvest microalgae with the cationic surfactant (CTAB), and the harvesting efficiency was more than 90% under optimal experimental conditions.

5. Economic analysis of microalgal harvesting using foam flotation The harvesting cost is an important index to be considered in microalgal foam flotation, which determines the feasibility of this method for large-scale microalgal harvesting. The cost of microalgal foam flotation includes two main parts: the cost of flotation reagents and the energy consumption of the flotation device. The flotation reagents

4.2. Pneumatic foam flotation for microalgal harvesting Pneumatic foam flotation is the earliest type of foam flotation applied for harvesting microalgae [38], which uses porous materials such as microporous ceramics for bubble generation. It is generally performed with a compressed air system (1,2), a separation column (3) and a porous sparger (4), as illustrated in Fig. 6. In pneumatic foam flotation, air is continuously supplied by the compressed air system and dispersed into bubbles by the porous sparger. Then collision between the particle (microalgal cell) and bubble is induced by the countercurrent contact. Thus, pneumatic foam flotation does not require a mechanical agitator and thus offers the advantages of simple structure, low energy consumption and a static separation flow field. The bubble properties (size and number) are mainly determined by the pore diameter and distance of the porous sparger, airflow velocity, pressure and liquid surface tension [91]. Spargers with a small pore diameter can generate small bubbles, and the bubble coalescence can be restrained by appropriately increasing the pore distance. Additionally, low airflow velocity or pressure results in fewer bubbles, whereas excessive airflow velocity or pressure generates a jet air stream without bubbles.

Fig. 5. Machine-stirred foam flotation for microalgal harvesting. 183

Biomass and Bioenergy 120 (2019) 176–188

H. Zhang, X. Zhang

m−3) [96], electro-flotation (3.84 kWh m−3) [97], filtration (2.06 kWh m−3) [98] and DAF (1.5 kWh m−3) [99]. Coward et al. [21] evaluated the cost of foam flotation for harvesting microalgae through calculating the theoretical work energy consumption of the air compressor (50% of energy exchange efficiency) and found that this method consumed 0.015 kWh m−3, but they did not consider the energy consumed by pump transport and collector dispersion. However, this result indicated that the total energy consumption of microalgal foam flotation can be further reduced by adopting the optimum bubble generation method. A comparison of the efficiency and energy consumption of foam flotation with those of common harvesting technologies [11,20,21,96,97,99] is shown in Table 4. Foam flotation exhibited high efficiency and low cost for microalgal harvesting, and thus may be the most promising harvesting technology for microalgae on a large scale. According to Table 5, the total cost of microalgal foam flotation (0.105 $ kg−1 DW) was mainly composed of energy and collector (CTAB) costs, and these two parts of the cost were 0.028 and 0.077 $ kg−1 DW, respectively. Considering the harvesting efficiency of 98.6%, the total cost of microalgal harvesting using a batch foam flotation system at the pilot scale was estimated to be approximately 0.11 $ kg−1 DW. Therefore, it is suggested that foam flotation is economically feasible for harvesting microalgae for biofuels. Additionally, it should be noted that the total cost of this method was dominated by the collector cost, which accounted for 73.33%. Thus, improvement in the collector adsorption efficiency or the selection of more economical collectors should be addressed to reduce the cost of microalgal foam flotation.

Fig. 6. Pneumatic foam flotation column for microalgal harvesting: (1) air compressor, (2) air storage tank, (3) flotation column, (4) sparger.

6. Challenges and perspectives of microalgal harvesting using foam flotation As discussed above, foam flotation exhibits great potential for largescale microalgal harvesting because of the simple process flow, small space requirements and few mechanical components. Foam flotation can realize high harvesting efficiency and a high enrichment ratio while using low energy. However, the principle of foam flotation is based on the interface interaction between particles and bubbles, and its performance is influenced by many factors such as the surface physical and chemical properties of microalgal cells and bubbles and the solution chemistry conditions. Most importantly, microalgal cells are living organisms with specific properties that differ from those of mineral particles, such as much more diluted concentrations and variations in cellular characteristics and medium properties. For the development of feasible foam flotation techniques and processes for harvesting microalgae on a commercial scale, numerous constraints must be overcome. The perspectives of microalgal harvesting using foam flotation are presented in Fig. 8.

Fig. 7. Jet foam flotation column for microalgal harvesting: (1) pump, (2) bubble generator, (3) flotation column.

generally include the collector, regulator (pH regulator: HCl or NaOH) and frother. In addition, some quaternary ammonium salts, such as CTAB, DAH and SDS simultaneously improve capture and froth performance. The energy costs mainly include the mechanical agitator (flotation reagent dispersion) and bubble generator and can be calculated from the power consumption. It is still too early to accurately calculate the cost of microalgal harvesting using foam flotation. However, estimates can be made for the cost of the main processes in the microalgal foam flotation to provide insight into the economic feasibility of this method. In this study, the cost of microalgal foam flotation was calculated at the pilot scale using a 1000 L batch foam machinery stirring foam flotation system to harvest Scenedesmus acuminatus, and the key parameters were based on our experimental results at the laboratory scale, as listed in Table 2. Other parameters are selected according to references [95]. The energy consumption calculation for each process and the results are shown in Table 3. The results demonstrated that using foam flotation for harvesting 1000 L of microalgae consumed a total energy of 0.46 kWh, which was more cost effective than centrifugation (8 kWh

Table 2 Summary of the key parameters used for the economic analysis of microalgal harvesting using foam flotation.

184

Parameters

Values

Initial microalgal concentration Initial pH of microalgal solution Stirring time Flotation time Flotation pH CTAB Harvesting efficiency Concentration factor Feed Pump (40-125-1-A)a Agitator (XB-1200)a Machinery stirring foam flotation machine (XCF-1)a Froth paddlea CTAB (industrial grade) priceb Electricity pricec

1.5 g L−1 6.5 ± 0.2 1 min 3 min 6.5 ± 0.2 10 mg g−1 DW 98.6% 25.7 1.1 kW h−1 3.0 kW h−1 5.5 kW h−1 0.75 kW h−1 7700 $ t−1 0.07 $ kWh−1

Biomass and Bioenergy 120 (2019) 176–188

H. Zhang, X. Zhang

Table 3 Allocations of the energy consumption of microalgal harvesting using foam flotation. Energy consumption calculation

Values

Pump energy consumed Agitator energy consumed Flotation machine energy consumed Froth paddle energy consumed Total energy consumed Total energy consumed per 1 kg microalgal biomass DW

0.09 kWh 0.05 kWh 0.28 kWh 0.04 kWh 0.46 kWh 0.31 kWh

Table 5 Calculated cost of microalgal harvesting using foam flotation. Cost calculation

Values

Energy cost CTAB cost Total cost Total cost based on the harvesting efficiency

m−3 m−3 m−3 m−3 m−3 kg−1 DW

0.028 0.077 0.105 0.106

$ $ $ $

Proportion −1

kg kg−1 kg−1 kg−1

DW DW DW DW

26.67% 73.33% – 100%

characteristics of collectors on mineral surfaces. These detection and analysis techniques may also be appropriate for exploring the interactions between microalgal cells and collectors, which will guide collector screening and synthesis.

6.1. Environmentally friendly collectors: screening, synthesis, recovery and recycling

6.3. Collision and attachment between microalgal cells and bubbles: size matching relation and interfacial interactions

In microalgal foam flotation, collectors such as CTAB are commonly used to improve the floatability of microalgal cells, and collector consumption consists of the 73.33% of the total harvesting cost as shown in the aboveeconomic analysis. However, few studies focus on the effects of collectors on medium recycling and the downstream processing of microalgal biomass for biofuels and bioproducts, which are critical aspects that need to be addressed in large-scale harvesting. Therefore, efforts need to be made to screen or synthesize environmentally friendly and economical collectors (i.e., bio-collectors) by comprehensively considering their adsorption mechanisms on the microalgal cells, synthetic principles and influences on the medium recycling as well as the subsequent downstream processing of microalgal biomass. Additional collector recovery and recycling techniques to purify the microalgal biomass and reduce the harvesting cost should also be addressed [100].

According to the collision and attachment processes between the microalgal cells and bubbles, the collision, attachment and detachment efficiencies are directly influenced by the size and interfacial interactions of the microalgal cells and bubbles. The size determines the collision, attachment and detachment efficiencies between microalgal cells and bubbles, and interfacial interactions determine the stability of attachment, which is closely related to detachment efficiency. According to Han et al. [45,108], the optimum bubble size depended on the particle size. There are size matching relations between bubbles and particles that govern the optimum flotation performance. Most of these related studies were carried out by theoretical derivation or by using single particle-bubble model [46,108], which may not perfectly fit the actual situation. Therefore, the size matching model between microalgal cells and bubbles should be established by the overall consideration of theoretical models and advanced analytical testing techniques (e.g., high-speed dynamic systems) for various sizes and shapes of microalgal production species. Leja et al. [109] reported that the interfacial interactions between mineral particles and bubbles mainly include hydrophobic interaction and electrostatic adherence. Nevertheless, there is limited literature on the interface interactions between microalgal cells and bubbles in microalgal foam flotation. Coward et al. [36] presented two hypotheses to describe the interactions between bubbles and microalgal cells when a cationic collector (CTAB) was used as a collector, as shown in Fig. 9. The first hypothesis is that the cationic collector changes the bubble charge from negative to positive, and then the positively charged bubbles attract the negatively charged cells by the electrostatic interaction (Fig. 9a). The other hypothesis predicts that cationic surfactant first adsorbs on the microalgal cells by electrostatic interaction, improving the hydrophobicity of the microalgal cells, and the cells then attach to the bubbles by hydrophobic interactions (Fig. 9b). However, neither of these hypotheses regarding the interaction between bubbles and microalgal cells has not been proven, and thus, further studies need to be carried out to explicitly understand the interface interactions

6.2. Adsorption mechanism and characteristics of collectors on microalgal cells The hydrophobization of microalgal cells is the precondition for microalgal harvesting using foam flotation. Therefore, revealing the adsorption mechanism between microalgal cells and collectors would improve the understanding of microalgal foam flotation. In mineral foam flotation, the adsorption mechanisms between mineral particles and collectors mainly involve chemical and physical (electrostatic and hydrogen-bond interaction) adsorption [101]. Additionally, adsorption characteristics, such as the adsorption amount and morphology of the adsorption layer, are closely related to the flotation performance and are strongly influenced by the surface properties of the particles, collector type and concentration, and solution chemical conditions [102]. However, such studies have not yet been reported in microalgal foam flotation. Fourier transform infrared spectroscopy (FTIR) [103], zeta potential analyzer [104], ultraviolet spectroscopy [105], high-performance liquid chromatography (HPLC) [106] and ion chromatography (IC) [107] can be used to measure the adsorption mechanisms and

Table 4 Comparison of the efficiency and energy consumption of foam flotation with those of common harvesting technologies. Harvesting technology

Energy consumption (kWh m−3)

Harvesting efficiency (HE), Total suspended solids (TSS) or Concentration factor (CF)

Remark

Centrifugation Filtration Flocculation-sedimentation Flocculation-dissolved air flotation Electrolytic flocculation Foam flotation Foam flotation (this study)

8.0 2.06 0.1 1.5

HE > 95% TSS 12% TSS 5%–27% TSS 0.5%–1.5% HE > 95% TTS 5%

High efficiency, extensive energy consumption Membrane fouling and high cost Low energy consumption, long separation time High efficiency and energy consumption

3.84 0.015 0.46

HE > 90% HE > 96% TTS 1.4–2.4 HE 98.6% CF 25.6

Electrode consumption High efficiency and low energy consumption High efficiency; Total energy consumption including pump, agitator, foam flotation machine and froth paddle are calculated.

185

Biomass and Bioenergy 120 (2019) 176–188

H. Zhang, X. Zhang

Fig. 8. An illustrative flow diagram of the proposed microalgal harvesting process using foam flotation.

Induction2015EZ, Oil Sands Environmental Development & Services Inc) [111,112]. It was also reported that atomic force microscopy (AFM) could be used to study the hydrophobic force and DLVO forces between particles and bubbles [113,114], as well as the thickness of the liquid film [115]. 6.4. Development of novel foam flotation devices for microalgal harvesting Although foam flotation has been applied to harvest microalgal biomass for several decades, there is no literature on any specialized device for the foam flotation of microalgae and most studies on microalgal foam flotation have been carried out by using mineral flotation devices at the laboratory scale [21,30,39]. The performances of flotation devices can directly influence the adsorption of microalgal cellcollector, bubble generation (size, number and energy consumption), the collision and attachment efficiency between microalgal cells and bubbles, and the separation environment (detachment efficiency and foam height), which further affect the flotation performance (harvesting efficiency and concentration factor) and cost (flotation reagents and energy consumption). Additionally, flotation operates via multiphase flow, and the flotation performance is directly impacted by the hydrodynamics of the flotation device [48,116]. The collision efficiency can be improved by a turbulent flow, and cell-bubble detachment can be reduced by a static separation environment. Therefore, it is necessary to comprehensively consider the collision, attachment and detachment efficiencies, as well as the harvesting costs, to develop and optimize foam flotation devices for economical and efficient microalgal harvesting.

Fig. 9. The two proposed hypotheses regarding interface interactions between microalgal cells and bubbles [36].

between microalgal cells and bubbles. Some parameters, such as the surface properties of microalgal cells (zeta potential and hydrophobicity) and bubbles (zeta potential), induction time, adsorption force and thickness of the liquid film may be measured to understand the interface interactions between bubbles and microalgal cells. A contact angle meter and zeta potential meter were applied to measure the hydrophobicity and zeta potential of microalgal cells respectively [41, 110]. The micro-electrophoretic technique could be used to measure the zeta potential of bubbles [78]. The induction time, which reflects the attachment efficiency, begins with the first contact of the bubble and particle, proceeds through the thinning and rupturing of the liquid film and the formation of the wet boundary of the gas-liquid-solid, and ends with stable attachment between the particle and bubble, which can be measured by an induction timer (e.g.,

7. Conclusions Foam flotation is a promising technique for microalgal harvesting 186

Biomass and Bioenergy 120 (2019) 176–188

H. Zhang, X. Zhang

[24] B.V. Derjaguin, S.S. Dukhin, Theory of flotation of small and medium-size particles, Prog. Surf. Sci. 43 (1) (1993) 241–266. [25] J. Ralston, Bubble-particle capture, Flotation (2000) 1464–1471. [26] D. Hewitt, D. Fornasiero, J. Ralston, Bubble–particle attachment, J. Chem. Soc., Faraday Trans. 91 (13) (1995) 1997–2001. [27] Z.F. Dai, D. Fornasiero, J. Ralston, Particle-bubble attachment in mineral flotation, J. Colloid Interface Sci. 217 (1) (1999) 70–76. [28] Z. Shen, Y.P. Li, H. Wen, X.Y. Ren, J. Liu, L.W. Yang, Investigation on the role of surfactants in bubble-algae interaction in flotation harvesting of Chlorella vulgaris, Sci. Rep. 8 (2018). [29] H. Wen, Y.P. Li, Z. Shen, X.Y. Ren, W.J. Zhang, J. Liu, Surface characteristics of microalgae and their effects on harvesting performance by air flotation, Int. J. Agric. Biol. Eng. 10 (1) (2017) 125–133. [30] S. Garg, L. Wang, P.M. Schenk, Effective harvesting of low surface-hydrophobicity microalgae by froth flotation, Bioresour. Technol. 159 (2014) 437–441. [31] H. Kwon, M. Lu, E.Y. Lee, J. Lee, Harvesting of microalgae using flocculation combined with dissolved air flotation, Biotechnol. Bioproc. Eng. 19 (1) (2014) 143–149. [32] J. Zhang, Particle Size Distribution in Dissolved Air Flotation Process for Drinking Water Treatment, Department of Geological and Civil Engineering, University of Manitoba, Winnipeg Manitoba, 2005, p. 82. [33] P.H. Smith, W.H. Funk, D.E. Proctor, Froth flotation for harvesting Chlorella algae, Northwest Sci. 42 (4) (1968) 165–171. [34] J.K. Edzwald, Algae, bubbles, coagulants, and dissolved air flotation, Water Sci. Technol. 27 (10) (1993) 67–81. [35] D.H. Kwak, M.S. Kim, Flotation of algae for water reuse and biomass production: role of zeta potential and surfactant to separate algal particles, Water Sci. Technol. 72 (5) (2015) 762–769. [36] T. Coward, J.G.M. Lee, G.S. Caldwell, Harvesting microalgae by CTAB-aided foam flotation increases lipid recovery and improves fatty acid methyl ester characteristics, Biomass Bioenergy 67 (2014) 354–362. [37] P.E. Wiley, K.J. Brenneman, A.E. Jacobson, Improved algal harvesting using suspended air flotation, Water Environ. Res. 81 (7) (2009) 702–708. [38] G.V. Levin, A. Gibor, J.R. Clendenning, F.D. Bogar, Harvesting of algae by froth flotation, Appl. Microbiol. 10 (2) (1962) 169 &. [39] J.C. Liu, Y.M. Chen, Y.-H. Ju, Separation of algal cells from water by column flotation, Separ. Sci. Technol. 34 (11) (1999) 2259–2272. [40] T. Coward, J.G.M. Lee, G.S. Caldwell, The effect of bubble size on the efficiency and economics of harvesting microalgae by foam flotation, J. Appl. Phycol. 27 (2) (2015) 733–742. [41] L. Xia, H.Q. Li, S.X. Song, Cell surface characterization of some oleaginous green algae, J. Appl. Phycol. 28 (4) (2016) 2323–2332. [42] T.T. Bui, S.-N. Nam, M. Han, Micro-bubble flotation of freshwater algae: a comparative study of differing shapes and sizes, Separ. Sci. Technol. 50 (7) (2015) 1066–1072. [43] T.T. Chau, W.J. Bruckard, P.T. Koh, A.V. Nguyen, A review of factors that affect contact angle and implications for flotation practice, Adv. Colloid Interface Sci. 150 (2) (2009) 106–115. [44] W. Xia, Role of particle shape in the floatability of mineral particle: an overview of recent advances, Powder Technol. 317 (2017) 104–116. [45] M. Han, T.-I. Kim, J. Kim, Effects of floc and bubble size on the efficiency of the dissolved air flotation (DAF) process, Water Sci. Technol. 56 (10) (2007) 109–115. [46] Z.F. Dai, D. Fornasiero, J. Ralston, Particle-bubble collision models - a review, Adv. Colloid Interface Sci. 85 (2–3) (2000) 231–256. [47] A.V. Nguyen, New method and equations for determining attachment tenacity and particle size limit in flotation, Int. J. Miner. Process. 68 (1) (2003) 167–182. [48] R.H. Yoon, The role of hydrodynamic and surface forces in bubble–particle interaction, Int. J. Miner. Process. 58 (1) (2000) 129–143. [49] W.A. Ducker, Z.G. Xu, J.N. Israelachvili, Measurements of hydrophobic and DLVO forces in bubble-surface interactions in aqueous solutions, Langmuir 10 (9) (1994) 3279–3289. [50] A. Ozkan, H. Berberoglu, Physico-chemical surface properties of microalgae, Colloid Surf. B-Biointerfaces 112 (2013) 287–293. [51] S. Garg, L. Wang, P.M. Schenk, Flotation separation of marine microalgae from aqueous medium, Separ. Purif. Technol. 156 (2015) 636–641. [52] S.-K. Kam, J. Gregory, The interaction of humic substances with cationic polyelectrolytes, Water Res. 35 (15) (2001) 3557–3566. [53] P. Mocchiutti, M.A. Zanuttini, Key considerations in the determination of polyelectrolyte concentration by the colloidal titration method, Bioresources 2 (3) (2007) 399–407. [54] M.-S. Kim, D.-H. Kwak, Effect of zeta potential on collision-attachment coefficient and removal efficiency for dissolved carbon dioxide flotation, Environ. Eng. Sci. 34 (4) (2017) 272–280. [55] W. Phoochinda, D.A. White, Removal of algae using froth flotation, Environ. Technol. 24 (1) (2003) 87–96. [56] H.A. Kurniawati, S. Ismadji, J.C. Liu, Microalgae harvesting by flotation using natural saponin and chitosan, Bioresour. Technol. 166 (2014) 429–434. [57] R.H. Crist, K. Oberholser, J. McGarrity, D.R. Crist, J.K. Johnson, J.M. Brittsan, Interaction of metals and protons with algae. 3. Marine algae, with emphasis on lead and aluminum, Environ. Sci. Technol. 26 (3) (1992) 496–502. [58] C.J. Tien, Biosorption of metal ions by freshwater algae with different surface characteristics, Process Biochem. 38 (4) (2002) 605–613. [59] S. Hadjoudja, V. Deluchat, M. Baudu, Cell surface characterisation of Microcystis aeruginosa and Chlorella vulgaris, J. Colloid Interface Sci. 342 (2) (2010) 293–299. [60] L. Xia, R. Huang, Y.T. Li, S.X. Song, The effect of growth phase on the surface

with the advantages of high efficiency and low energy consumption. Nevertheless, the application of foam flotation to microalgal harvesting is still at an early stage, as most of the current applications are focused only on the process optimization. Therefore, to develop efficient, costeffective and environmentally sustainable microalgal harvesting, more investigations should be carried out to better understand the processes involved in microalgal foam flotation, including exploring low cost and environmentally friendly collectors, disclosing the interface interaction mechanisms of microalgal cell-collector-bubble and the developing of novel devices. Acknowledgments The authors gratefully acknowledge the support of the Doctor Research Foundation of Southwest University of Science and Technology (14zx7130) and the Foundation of Key Laboratory of Solid Waste Treatment and Resource Recycle Ministry of Education for Professional Innovation Research Team (14tdgk02). This work was also partially supported by the One-Hundred Scholars Award from the Chinese Academy of Sciences (Y62305-1-Z01). References [1] L. Tang, Strategic choice for national adjustment of renewable energy in China, in: P. Yarlagadda (Ed.), Proceedings of the 3rd International Conference on Advances in Energy and Environmental Science 20152015, pp. 975-979. [2] M.F. Demirbas, Biofuels from algae for sustainable development, Appl. Energy 88 (10) (2011) 3473–3480. [3] J. Milano, H.C. Ong, H.H. Masjuki, W.T. Chong, M.K. Lam, P.K. Loh, V. Vellayan, Microalgae biofuels as an alternative to fossil fuel for power generation, Renew. Sustain. Energy Rev. 58 (2016) 180–197. [4] C.A. Laamanen, G.M. Ross, J.A. Scott, Flotation harvesting of microalgae, Renew. Sustain. Energy Rev. 58 (2016) 75–86. [5] Y. Jiang, W. Zhang, J. Wang, Y. Chen, S. Shen, T. Liu, Utilization of simulated flue gas for cultivation of Scenedesmus dimorphus, Bioresour. Technol. 128 (2013) 359–364. [6] J.-P. Cadoret, O. Bernard, Lipid biofuel production with microalgae: potential and challenges, J. Soc. Biol. 202 (3) (2008) 201–211. [7] T.M. Mata, A.A. Martins, N.S. Caetano, Microalgae for biodiesel production and other applications: a review, Renew. Sustain. Energy Rev. 14 (1) (2010) 217–232. [8] J.E. Coons, D.M. Kalb, T. Dale, B.L. Marrone, Getting to low-cost algal biofuels: a monograph on conventional and cutting-edge harvesting and extraction technologies, Algal Res. Biomass Biofuel. Bioprod. 6 (2014) 250–270. [9] E.M. Grima, E.H. Belarbi, F.G.A. Fernandez, A.R. Medina, Y. Chisti, Recovery of microalgal biomass and metabolites: process options and economics, Biotechnol. Adv. 20 (7–8) (2003) 491–515. [10] J.B.K. Park, R.J. Craggs, A.N. Shilton, Wastewater treatment high rate algal ponds for biofuel production, Bioresour. Technol. 102 (1) (2011) 35–42. [11] N. Uduman, Y. Qi, M.K. Danquah, G.M. Forde, A. Hoadley, Dewatering of microalgal cultures: a major bottleneck to algae-based fuels, J. Renew. Sustain. Energy 2 (1) (2010). [12] K.Y. Show, D.J. Lee, J.S. Chang, Algal biomass dehydration, Bioresour. Technol. 135 (2013) 720–729. [13] C. Banerjee, S. Ghosh, G. Sen, S. Mishra, P. Shukla, R. Bandopadhyay, Study of algal biomass harvesting through cationic cassia gum, a natural plant based biopolymer, Bioresour. Technol. 151 (2014) 6–11. [14] M.R. Teixeira, M.J. Rosa, Comparing dissolved air flotation and conventional sedimentation to remove cyanobacterial cells of Microcystis aeruginosa, Separ. Purif. Technol. 52 (1) (2006) 84–94. [15] X. Zhang, Q. Hu, M. Sommerfeld, E. Puruhito, Y. Chen, Harvesting algal biomass for biofuels using ultrafiltration membranes, Bioresour. Technol. 101 (14) (2010) 5297–5304. [16] S. Babel, S. Takizawa, Microfiltration membrane fouling and cake behavior during algal filtration, Desalination 261 (1–2) (2010) 46–51. [17] J. Rubio, M.L. Souza, R.W. Smith, Overview of flotation as a wastewater treatment technique, Miner. Eng. 15 (3) (2002) 139–155. [18] J.K. Edzwald, Dissolved air flotation and me, Water Res. 44 (7) (2010) 2077–2106. [19] K.A. Matis, G.P. Gallios, K.A. Kydros, Separation of fines by flotation techniques, Sep. Technol. 3 (2) (1993) 76–90. [20] S. Garg, Y. Li, L. Wang, P.M. Schenk, Flotation of marine microalgae: effect of algal hydrophobicity, Bioresour. Technol. 121 (2012) 471–474. [21] T. Coward, J.G.M. Lee, G.S. Caldwell, Development of a foam flotation system for harvesting microalgae biomass, Algal Res. Biomass Biofuel. Bioprod. 2 (2) (2013) 135–144. [22] T. Ndikubwimana, J. Chang, Z. Xiao, W. Shao, X. Zeng, I.S. Ng, Y. Lu, Flotation: a promising microalgae harvesting and dewatering technology for biofuels production, Biotechnol. J. 11 (3) (2016) 315–326. [23] J. Ralston, D. Fornasiero, R. Hayes, Bubble-particle attachment and detachment in flotation, Int. J. Miner. Process. 56 (1–4) (1999) 133–164.

187

Biomass and Bioenergy 120 (2019) 176–188

H. Zhang, X. Zhang

[61]

[62]

[63]

[64] [65]

[66] [67] [68] [69]

[70]

[71] [72] [73] [74]

[75]

[76]

[77]

[78]

[79] [80] [81] [82] [83] [84]

[85]

[86] [87] [88] [89]

(1–4) (1989) 77–99. [90] C.W. Bakker, C.J. Meyer, D.A. Deglon, The development of a cavern model for mechanical flotation cells, Miner. Eng. 23 (11–13) (2010) 968–972. [91] W. Kracht, C.O. Gomez, J.A. Finch, Controlling bubble size using a frit and sleeve sparger, Miner. Eng. 21 (9) (2008) 660–663. [92] Z. Yanqin, A. Caihong, Y. Hongli, D. Lianping, F. Minqiang, Research on longitudinal homogeneity of air bubble in jet flotation column, J. China Coal Soc. (1) (2009) 95–99. [93] L.J. iongtian, W. Yongtian, Study on performance of self-absorbing microbubble generator, J. China Inst. Min. Technol. 27 (1) (1998) 27–31. [94] L. Li, J.-t. Liu, Y.-t. Wang, Y.-j. Cao, H.-j. Zhang, H.-s. Yu, Experimental research on anionic reverse flotation of hematite with a flotation column, in: S. Ge, J. Liu, C. Guo (Eds.), Proceedings of the International Conference on Mining Science & Technology2009, pp. 791-798. [95] T.G. Hicks, Standard Handbook of Engineering Calculations, fifth ed., McGrawHill Education, New York, 2014. [96] M.K. Danquah, L. Ang, N. Uduman, N. Moheimani, G.M. Forde, Dewatering of microalgal culture for biodiesel production: exploring polymer flocculation and tangential flow filtration, J. Chem. Technol. Biotechnol. 84 (7) (2009) 1078–1083. [97] R. Misra, A. Guldhe, P. Singh, I. Rawat, T.A. Stenström, F. Bux, Evaluation of operating conditions for sustainable harvesting of microalgal biomass applying electrochemical method using non sacrificial electrodes, Bioresour. Technol. 176 (Supplement C) (2015) 1–7. [98] M.K. Danquah, L. Ang, N. Uduman, N. Moheimani, G.M. Fordea, Dewatering of microalgal culture for biodiesel production: exploring polymer flocculation and tangential flow filtration, J. Chem. Technol. Biotechnol. 84 (7) (2009) 1078–1083. [99] M.K. Weschler, W.J. Barr, W.F. Harper, A.E. Landis, Process energy comparison for the production and harvesting of algal biomass as a biofuel feedstock, Bioresour. Technol. 153 (Supplement C) (2014) 108–115. [100] L. Yang, L. Wang, H. Zhang, C. Li, X. Zhang, Q. Hu, A novel low cost microalgal harvesting technique with coagulant recovery and recycling, Bioresour. Technol. 266 (2018) 343–348. [101] J. Tian, L. Xu, W. Deng, H. Jiang, Z. Gao, Y. Hu, Adsorption mechanism of new mixed anionic/cationic collectors in a spodumene-feldspar flotation system, Chem. Eng. Sci. 164 (2017) 99–107. [102] A.C. Partridge, G.W. Smith, Flotation and adsorption characteristics of the hematite-dodecylamine-starch system, Can. Metall. Q. 10 (3) (1971) 229–+. [103] J.O. Leppinen, FTIR and flotation investigation of the adsorption of ethyl xanthate on activated and non-activated sulfide minerals, Int. J. Miner. Process. 30 (3) (1990) 245–263. [104] A. Vidyadhar, K. Hanumantha Rao, Adsorption mechanism of mixed cationic/ anionic collectors in feldspar-quartz flotation system, J. Colloid Interface Sci. 306 (2) (2007) 195–204. [105] G. Fairthorne, D. Fornasiero, J. Ralston, Interaction of thionocarbamate and thiourea collectors with sulphide minerals: a flotation and adsorption study, Int. J. Miner. Process. 50 (4) (1997) 227–242. [106] M.J. Wu, C.S. Zhou, X.A. Xiong, Y. Wang, Determination of high performance liquid chromatography for ore flotation collector, Hunan Nonferrous Met. 11 (2) (1995) 53–57. [107] T.N. Khmeleva, W. Skinner, D.A. Beattie, Depressing mechanisms of sodium bisulphite in the collectorless flotation of copper-activated sphalerite, Int. J. Miner. Process. 76 (1) (2005) 43–53. [108] M.Y. Han, Modeling of DAF: the effect of particle and bubble characteristics, J. Water Supply Res. Technol. - Aqua 51 (1) (2002) 27–34. [109] J. Leja, J.H. Schulman, Flotation theory: molecular interactions between frothers and collectors at solid–liquid–air interfaces, Trans. Am. Inst. Min. Metall. Eng. 199 (2) (1954) 221–228. [110] M.A.S. Alkarawi, G.S. Caldwell, J.G.M. Lee, Continuous harvesting of microalgae biomass using foam flotation, Algal Res. 36 (2018) 125–138. [111] R.-H. Yoon, J.L. Yordan, Induction time measurements for the quartz—amine flotation system, J. Colloid Interface Sci. 141 (2) (1991) 374–383. [112] S.-j. Chen, X.-x. Tao, Y.-c. Yang, L. Chen, Z.-l. Yang, Experimental study on induction time of shendong low rank coal, Coal Technol. 35 (7) (2016) 319–321. [113] G. Gillies, M. Kappl, H.J. Butt, Direct measurements of particle-bubble interactions, Adv. Colloid Interface Sci. 114–115 (2005) 165–172. [114] A.V. Nguyen, J. Nalaskowski, J.D. Miller, H.-J. Butt, Attraction between hydrophobic surfaces studied by atomic force microscopy, Int. J. Miner. Process. 72 (1–4) (2003) 215–225. [115] A. Doppenschmidt, H.J. Butt, Measuring the thickness of the liquid-like layer on ice surfaces with atomic force microscopy, Langmuir 16 (16) (2000) 6709–6714. [116] H. Schubert, C. Bischofberger, On the hydrodynamics of flotation machines, Int. J. Miner. Process. 5 (2) (1978) 131–142.

properties of three oleaginous microalgae (Botryococcus sp FACGB-762, Chlorella sp XJ-445 and Desmodesmus bijugatus XJ-231), PloS One 12 (10) (2017) 11. X. Zhang, P. Amendola, J.C. Hewson, M. Sommerfeld, Q. Hu, Influence of growth phase on harvesting of Chlorella zofingiensis by dissolved air flotation, Bioresour. Technol. 116 (2012) 477–484. Q. Hu, M. Sommerfeld, E. Jarvis, M. Ghirardi, M. Posewitz, M. Seibert, A. Darzins, Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances, Plant J. 54 (4) (2008) 621–639. R. Henderson, S.A. Parsons, B. Jefferson, The impact of algal properties and preoxidation on solid–liquid separation of algae, Water Res. 42 (8) (2008) 1827–1845. R.K. Henderson, S.A. Parsons, B. Jefferson, Successful removal of algae through the control of zeta potential, Separ. Sci. Technol. 43 (7) (2008) 1653–1666. X. Zhang, L. Wang, M. Sommerfeld, Q. Hu, Harvesting microalgal biomass using magnesium coagulation-dissolved air flotation, Biomass Bioenergy 93 (2016) 43–49. A. Demirbas, Use of algae as biofuel sources, Energy Convers. Manag. 51 (12) (2010) 2738–2749. S. Yan, J.Q. Zhang, W.Z. Diao, Flotation reagent progress and application overview, Appl. Mech. Mater. 441 (2013) 76–79. H. Sis, S. Chander, Reagents used in the flotation of phosphate ores: a critical review, Miner. Eng. 16 (7) (2003) 577–585. E.W. Giesekke, A review of spectroscopic techniques applied to the study of interactions between minerals and reagents in flotation systems, Int. J. Miner. Process. 11 (1) (1983) 19–56. A. Csordas, J.-K. Wang, An integrated photobioreactor and foam fractionation unit for the growth and harvest of Chaetoceros spp. in open systems, Aquacult. Eng. 30 (1) (2004) 15–30. R.I.L. Guthrie, A.V. Bradshaw, Spherical capped gas bubbles rising in aqueous media, Chem. Eng. Sci. 28 (1) (1973) 191 &. H. Tsuge, S.-I. Hibino, The onset conditions of oscillatory motion of single gas bubbles rising in various liquids, J. Chem. Eng. Jpn. 10 (1) (1977) 66–68. R.H. Yoon, G.H. Luttrell, The effect of bubble size on fine particle flotation, Miner. Process. Extr. Metall. Rev. 5 (1–4) (1989) 101–122. A. Hassanzadeh, B.V. Hassas, S. Kouachi, Z. Brabcova, M.S. Ccedil, elik, Effect of bubble size and velocity on collision efficiency in chalcopyrite flotation, Colloid. Surface. A Physicochem. Eng. Aspect. 498 (2016) 258–267. Y.W. Xing, X.H. Gui, Y.J. Cao, Effect of bubble size on bubble-particle attachment and film drainage kinetics - a theoretical study, Powder Technol. 322 (2017) 140–146. L. Pan, S. Jung, R.-H. Yoon, A fundamental study on the role of collector in the kinetics of bubble–particle interaction, Int. J. Miner. Process. 106–109 (2012) 37–41. C. Yang, T. Dabros, D. Li, J. Czarnecki, J.H. Masliyah, Measurement of the zeta potential of gas bubbles in aqueous solutions by microelectrophoresis method, J. Colloid Interface Sci. 243 (1) (2001) 128–135. C. Oliveira, J. Rubio, Zeta potential of single and polymer-coated microbubbles using an adapted microelectrophoresis technique, Int. J. Miner. Process. 98 (1–2) (2011) 118–123. M. Han, S. Dockko, Zeta potential measurement of bubbles in DAF process and its effect on the removal efficiency, KSCE J. Civil Eng. 2 (4) (1998) 461–466. B.T. Arturo, P.G. Roberto, M.C. Diego, Zeta potential of air bubbles conditioned with typical froth flotation reagents, Int. J. Miner. Process. 140 (2015) 50–57. M.Y. Han, H.J. Ahn, M.S. Shin, S.R. Kim, The effect of divalent metal ions on the zeta potential of bubbles, Water Sci. Technol. 50 (8) (2004) 49–56. T.V. Subrahmanyam, E. Forssberg, Froth stability, particle entrainment and drainage in flotation — a review, Int. J. Miner. Process. 23 (1) (1988) 33–53. Y.S. Cho, J.S. Laskowski, Effect of flotation frothers on bubble size and foam stability, Int. J. Miner. Process. 64 (2) (2002) 69–80. A.K. Gupta, P.K. Banerjee, A. Mishra, P. Satish, Pradip, Effect of alcohol and polyglycol ether frothers on foam stability, bubble size and coal flotation, Int. J. Miner. Process. 82 (3) (2007) 126–137. C.P. Huang, J.R.S. Pan, S.H. Huang, Collision efficiencies of algae and kaolin in depth filter: the effect of surface properties of particles, Water Res. 33 (5) (1999) 1278–1286. Y.M. Chen, J.C. Liu, Y.-H. Ju, Flotation removal of algae from water, Colloids Surfaces B Biointerfaces 12 (1) (1998) 49–55. A.C.C. Pacheco, M.L. Torem, Influence of ionic strength on the removal of As5+ by adsorbing colloid flotation, Separ. Sci. Technol. 37 (15) (2002) 3599–3610. Z. Shen, Development history and trend of flotation cell, Nonferrous Met. (S1) (2011) 34–46. N. Ahmed, G.J. Jameson, Flotation kinetics, Miner. Process. Extr. Metall. Rev. 5

188