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Algal Research: Review Article
Algal Research: Review Article
Algal Research
journal homepage: www.elsevier.com/locate/algal
Review article
A R T I C LE I N FO A B S T R A C T
Keywords: Microalgae are considered as a potential and sustainable feedstock for the production of biofuels, fine chemicals,
Microalgae nutraceuticals, and cosmetics. This is accredited to their high lipid and carbohydrate content, fast growth and
Harvesting rapid CO2 sequestration ability. However, large volumes of feedstock are required to extract and process bio-
Review chemicals from microalgal biomass due to the small biomass to liquid ratio. This produces substantial challenges
Economic viability
in attaining a sustainable energy balance in microalgae-based products process operations. Additionally, the
Life cycle assessment
small size of microalgal cells along with their negatively charged cell surface and cell density similar to the
Technoeconomic analysis
growth medium produces challenges in microalgae harvesting. The high cost associated with microalgae har-
vesting is a major bottleneck for commercialization of algae-based industrial products. Hence, microalgae
harvesting is recognized as an area that needs to be explored and developed. This article aims to collate and
present an overview of current harvesting strategies such as physical, chemical, biological, electrical and
magnetic methods along with their future prospects. This review also highlights the evolution of microalgal
harvesting and elucidates the fundamental phenomena of each technology in relation to key physical parameters
such as morphology, size, density and surface charge. Besides throwing widespread light on various harvesting
methods, this review article has also presented their advantages and disadvantages. Life cycle assessment (LCA)
and technoeconomic analysis (TEA) was reviewed to assess the feasibility of various harvesting system for
commercial application based on the environmental and technoeconomic impacts. Hence, the vital proposals
provided in this review article would undeniably pave the way for choosing the appropriate harvesting strategy.
1. Introduction possess the potential to generate a considerable amount of oil per acre
as compared to other biofuel feedstock. Moreover, the land that is not
The rapid growth of population and advancement in technology suitable for crop cultivation can be used for growing microalgae [4].
may lead to a rise in global energy consumption from 550 EJ in 2020 to Microalgae are unicellular photosynthetic microorganisms that grow
865 EJ by 2040 [1]. The need for energy must be satiated to maintain very fast and has a thirst for carbon dioxide. The three key elements
pace with technological development. Primary energy sources include required for microalgal growth are light source (obtained from sun),
both renewable as well as non-renewable sources. Fossil fuel, which is a nutrients (mainly nitrogen, phosphorus and trace metals) [5] and a
non-renewable energy resource, is widely used to meet the global en- carbon source (derived from CO2). These are then stored in the cell
ergy demand. But, fossil fuel provides a finite amount of energy, and a tissues as carbohydrates, lipids, proteins and silica nanomaterials (in
significant amount of impact is imposed on the environment during its the case of diatom species) [6]. Microalgae biomass being rich in bio-
exploration and use [2]. A major portion of the world’s energy is pro- chemical composition favours the production of a broad spectrum of
duced and consumed by India. India, by producing 2.49% of the world’s marketable value-added products. The presence of triglycerides in mi-
total annual energy ranks seventh in terms of energy production [3]. croalgal lipids favours biodiesel production. A range of different in-
Research on microalgae as a feedstock for various products such as dustries can also use microalgal proteins and carbohydrates [7]. Pro-
biofuels, chemicals, pharmaceutical, aquaculture feed, and cosmetics ducts having high market value, such as β-carotene [8], PUFA such as
continues to increase because of the inherent advantages it holds over eicosapentaenoic acid and docosahexaenoic acid [9], and astaxanthin
other traditional feedstock. From bioenergy perspective, microalgae [10] can be obtained in low volumes from microalgae. Besides having
⁎
Corresponding author at: Centre for Energy, Indian Institute of Technology Guwahati, Guwahati 781 039, India
E-mail address: kmohanty@iitg.ac.in (K. Mohanty).
https://doi.org/10.1016/j.algal.2019.101683
Received 2 July 2019; Received in revised form 24 September 2019; Accepted 24 September 2019
2211-9264/ © 2019 Elsevier B.V. All rights reserved.
M. Roy and K. Mohanty Algal Research 44 (2019) 101683
the ability to produce bio-products, microalgae also help in bior- harvesting process [19].
emediation such as carbon dioxide sequestration [11], and the elim- Fouling is a major drawback that hinders the harvesting of micro-
ination of heavy metals from effluents [12]. The ability to produce algae through membrane filtration. Fouling occurs because microalgae
high-value products along with bioremediation capability confirms can produce biofilms as they possess extracellular organic matter
microalgae as the potential feedstock in industrial sectors. However, (EOM), mostly protein, polysaccharides or polysaccharide like sub-
microalgae-based production technologies suffer from several limita- stances, attached to their cells. The impact of EOM can be seen on the
tions at different stages of the upstream and downstream processes surface chemistry of mineral particles [24,25]. EOM either promotes or
[13]. Harvesting of algal biomass is one of the major bottlenecks during inhibits floc formation and chelating metal cations [26,27]. The con-
downstream processing, as it involves high energy input [14]. Almost centration of EOM is observed to vary widely from species to species.
80%–90% of the equipment cost is utilized for harvesting microalgal For example, in cyanobacteria Synechocystis, the EOM concentration is
biomass from open ponds [15]. found to be 1.8 mg L−1, whereas, for the green algae Chlorella, the EOM
This review article highlights the evolution of microalgal harvesting concentration is found to be 81 mg L-1 [16]. The concentration of EOM
strategies and elucidates the underlying phenomena of each technology is reported to increase with the age of microalgae culture. However, a
in relation to key physical parameters such as morphology, size, density depletion in the content of uronic acid inside the EOM is witnessed as
and surface charge. Apart from discussing various harvesting techni- the microalgal culture ages [21].
ques, this article also sums up the details of the experimental condi-
tions, which play a key role in the process itself. This will help provide 3. Microalgal harvesting strategies
firsthand knowledge to future researchers for selecting optimal ex-
perimental parameters for achieving maximum harvesting efficiency. Harvesting is a process of separating microalgal biomass from the
The environmental footprint resulting from the employment of several growth medium. The strategy employed for harvesting and dewatering
harvesting strategies is a concerning matter that has been analyzed the microalgae generally accounts for approximately 3%–30% of total
briefly in this article by using life cycle assessment (LCA). Moreover, biomass cost [28,29]. Thus, the economy of microalgal production is
technoeconomic analysis (TEA) has also been discussed to evaluate the significantly influenced by the harvesting technology [30]. As men-
economic feasibility of the harvesting processes. tioned earlier, several factors such as the cell age, shape, type, density
and size of the target microalgae and the significance of the end product
2. Physical properties of microalgae influence the selection of harvesting technology [28]. Typically a har-
vesting method which yields algal biomass with minimum moisture
A diverse range of microalgae (brown, red and green), cyano- content is preferred [14]. The high moisture content of harvested algal
bacteria and diatoms have been exploited to produce feedstock for food, biomass may also increase the cost of further processing [14]. Gen-
nutraceuticals, fuel and fine chemicals [7]. These microalgae, cyano- erally, microalgal harvesting involves two concentration steps. During
bacteria, and diatoms are found in different shapes and forms: spherical the primary harvesting, thickening procedure is applied where the
or filamentous, elongated and their cell size ranges from 0.5 to 200 μm. microalgal slurry is concentrated to around 2%–7% of total suspended
Moreover, single cells can combine to form more complex structures solids (TSS). This can be attained by applying either flotation, sedi-
such as filaments. The green algae Spirogyra, the cyanobacteria Ana- mentation, flocculation or a combination of flotation and sedimentation
baena and the diatom Melosira have the capability to develop chains of processes [20]. Thickening procedure is followed by a secondary de-
cells [16]. The Scenedesmus species came to spotlight because of its watering procedure, that results in the formation of an algal cake with
potential source of lipids for biodiesel production and high-value car- 15%–25% TSS, which can be attained by using centrifugation or fil-
otenoid. These Scenedesmus species generally manifest long spines in tration [31]. However, a secondary dewatering procedure requires
the colonies of two or four-cell coenobia [17]. Whereas, some species more energy as compared to primary thickening procedures. Currently,
such as Chlamydomonas reinhardtii are found to be flagellated and mo- microalgal cells are harvested either by physical, chemical, biological,
bile within the medium. Chlamydomonas reinhardtii has also been electrical or magnet-based methods. Some researchers have combined
highlighted as a potential strain used for genetic manipulation [18]. two or more of the above methods to harvest maximum microalgal
This wide range of physical characteristics exhibited by microalgae biomass. Table 1 shows a comparison of various harvesting techniques.
disturbs harvesting efficiency. For instance, flagellated cells evade
flocculation by swimming out of flocs, and the cells get easily damaged
when mechanical harvesting method is used [19]. 3.1. Physical methods
The cell surface charge or Zeta potential of microalgae is negative,
and it plays a vital role in the downstream processing. Gerardo et al. 3.1.1. Sedimentation
[20] reported that the zeta potential of microalgal cells can vary from In the process of sedimentation, gravitational forces entail the set-
− 2 mV to − 75 mV under the influence of chemical functional groups tling of the suspended algal cells from the medium of different density.
present in the cell surface, which changes with culture conditions and However, if the particle size or density difference is small, the separa-
cell age [21,22]. Moreover, ionization of certain chemical functional tion process may be reduced. The sedimentation principle can be well
groups on the microalgal cell surface, such as the amino and carboxyl explained by Stokes’ Law according to which the settling velocity is
groups, is involved in the charge and stabilization of microalgae sus- directly proportional to the square of the (Stokes’) radius of the cells
pensions [19]. Ionization of amino and carboxyl groups is greatly de- and the difference in density between the microalgal cells and the
pendent on pH, and these ionized functional groups influence the medium as given below [32]:
physicochemical features of microalgal cells [23]. 2 r2
The cell density of diatoms and green algae is reported to vary from Setting velocity = g (ρ − ρ1)
9 η s (1)
1070 kg m−3 to 1140 kg m-3, respectively [16]. Sedimentation, a
gravity-based separation process is highly influenced by the difference where, η denotes the fluid dynamic viscosity, r denotes the cell radius,
in solid-liquid/algae-medium density. The diameter of algal cells plays and ρs and ρl denote the solid and liquid densities.
a key role in the sedimentation process, as the size of the cell affects the Microalgal sedimentation is driven by a small density difference as
drag of the algal cells in the medium. Rapid settling can be observed if microalgae has a density nearly the same as that of saltwater and water
the effective cell size is enlarged by algal cell flocculation. Microalgal at 1025 kg m−3 [33]. The density of marine microalgae ranges between
cells containing high lipid and gas vesicles do not settle under the in- 1030 kg m−3 and 1100 kg m−3 [34], the density of marine diatom and
fluence of any gravitational force, thus, increasing the complexity of the dinoflagellates ranges between 1030 kg m−3 and 1230 kg m−3, the
2
M. Roy and K. Mohanty Algal Research 44 (2019) 101683
[75,149,150,151]
[42,115,150,154]
[45,47,149,150]
between 1040 kg m−3 and 1140 kg m−3 [35] and the density of cya-
[126,150,151]
[52,150,151]
[62,150,152]
[98,150,153]
[23,29,150]
[80,92,150]
nobacteria ranges between 1082 kg m−3 and 1104 kg m−3. The settling
velocity varies depending upon the type of microalgae. According to
Ref.
Unsuitable
Unsuitable
Unsuitable
Unsuitable
0.05 m day-1 respectively [36]. An experimental study found that the
Suitable
Suitable
Suitable
Suitable
Suitable
theoretical settling velocity of microalgae deviates from the observed
settling velocity [34,37].
Stokes’ law is valid only for spherical shapes, but most of the mi-
croalgae are found to exhibit different morphology [38]. Microalgae
Reusability of
Possible
Possible
Possible
Possible
Limited
Limited
Limited
Limited
them from settling from the euphotic zone [34]. In a study of 24 mi-
croalgae that ranged in size from 10 to 1000 μm, the settling rate was
observed to vary between 0.4 and 2.2 m day−1. But the study couldn’t
Microbial contamination
find a direct correlation between cell size and settling rates for diatoms
AOM and EOM released
Metal contamination
Metal contamination
Metal contamination
No toxicity
No toxicity
Chlorogonium.
The sedimentation rate not only varies among microalgae species
Medium
Medium
Medium
but also varies within the same species. Studies found that settling rates
High
High
High
High
Low
Low
might vary with light intensity [40] and nutrient content [41]. How-
ever, older cells (senescent cells) [34] and spore-forming cells have high
sinking rates [41]. It has been reported that lipid-rich microalgae have
consumption
low density, and hence the settling rate is less. The average density of
lipid is 860 kg m−3, protein 1300 kg m−3 and carbohydrate 1500 kg m-
Energy
3
High
High
[37].
Low
Low
Low
Low
Low
Low
Low
The sedimentation process has not been extensively used for settling
of microalgae [42] as the sedimentation rate of 4–5 μm sized micro-
Unfeasible for very small
algae in the large scale is very small [40]. In the case of microalgal
settling, cell recovery is meagre, i.e., 60%–65% [43]. Moreover, a large
Species specific
size microalgae
land area is required for constructing settling ponds and tanks [44]. A
study found that as the settlement process is time-consuming, high-
temperature environments may deteriorate most of the biomass pro-
duced [21]. But the energy consumed during the sedimentation process
Yes
Yes
No
No
No
No
No
No
0.1 kWh m−3 for obtaining 0.1%–1.5% dry microalgal biomass [45]. As
Medium
Short
Short
Short
Short
Short
Short
Long
Yes
No
No
No
No
No
No
No
Medium
High
High
High
High
High
High
High
Low
3.1.2. Centrifugation
The harvesting of biomass through centrifugation is based on the
application of centrifugal force to enhance the settling rate. The effi-
Magnetic particle assisted
difference between the microalgae biomass and the medium. The set-
Electroflocculation
harvesting
Centrifugation
Sedimentation
2 P
⎛ ds ⎞ = ω rΔρD2
⎝ dt ⎠c 18μ (2)
3
M. Roy and K. Mohanty Algal Research 44 (2019) 101683
where, ( )
ds
denotes the settling velocity of the cells (m s−1), Dp de- sedimentation [52]. Recovery of biomass via flotation is mainly de-
dt c
notes the cell diameter (m), r denotes the radial distance from cen- pendent on the low density of microalgae, as the low density of mi-
trifuge axis (m), μ denotes the medium viscosity (kg m−1), Δρ denotes croalgal cells facilitates them to float upwards more easily and rapidly
the difference between the density of cells and medium (kg m-3), and ω than to sediment downwards [19]. Some cyanobacteria such as Ana-
denotes the rotational velocity (s− 1). The total time, t, required to baena, Microcystis, and Spirulina possess gas vesicles which facilitates
settle a microalgae cell increases with the settling distances (settling them to float naturally [19]. Although some microalgae float naturally
path), s: due to its low density or presence of gas vesicles, incorporation of air
bubbles in the medium can also help in promoting flotation [52]. In
s 18μs most cases, like sedimentation process flocculants are required to be
t= =
ω2rΔρDP2
( )
ds
dt c (3) added to make the flotation effective [53]. A study found that large
flocs produced by combining organic and inorganic polymers facilitated
Centrifuges of various designs are available, the characteristics of flotation of marine microalgae, Isochrysis galbana [54]. Flocculation
the feed and the end-product requirement determines the selection flotation favours over sedimentation for the recovery of microalgal
between sedimentation centrifuges or filtration centrifuges. Usually, to biomass because of the low density of microalgal flocs as compared to
procure clarified liquid sedimentation centrifuges are used, while fil- microalgal cells [55].
tration centrifuges are utilized to obtain dry cake [19]. Harvesting of Based on the technique of bubble production, flotation processes are
microalgae biomass through centrifugation is much advantageous as classified as froth flotation, dispersed air flotation, dissolved air flota-
compared to other methods. Flocculants and chemicals free biomass tion and electrolytic flotation [47]. Froth flotation is a promising ap-
can be obtained through centrifugation. Harvesting of microalgae bio- proach for commercial-scale harvesting of microalgae. However, all the
mass through centrifugation is applicable to all types of microalgae surfactants employed for froth flotation are conventional monomeric
strains [48]. Harvesting through this process ensures a high recovery surfactants containing a single similar hydrophobic group in the mo-
rate. A study evaluated the cell viability and harvesting efficiency of lecule, which leads to low harvesting efficiency. Whereas, a novel Ge-
various microalgae species using three different centrifugation techni- mini surfactant, N,N′-bis(cetyldimethyl)-1,4-butane diammonium di-
ques: bottle centrifuge which operates at 1300 g-force, batch disc bromide (BCBD) consist of two traditional monomeric amphiphiles that
centrifuge which operates at 6000 g-force and the tubular bowl cen- are covalently connected by a spacer unit, resulting in a high harvesting
trifuge which operates at 13,000 g-force. The tubular bowl centrifuge, efficiency [56,57]. Fig. 1. depicts the schematics of microalgal froth
being operated at the highest g-force can achieve harvesting efficiency flotation using Gemini BCBD or cetyl trimethylammonium bromide
of nearly 100% for all species. However, some species such as Chaeto- (CTAB) as collector.
ceros muelleri and Isochrysis sp. are found to be more sensitive to high g- Dissolved air flotation (DAF) involves the generation of air bubbles
force. The bottle centrifuge, being operated at the lowest g-force is less that range in size from 10 to 100 μm with a mean size of 40 μm [53]. In
efficient. Nonetheless, this technique ensures 100% cell viability for all countries such as the USA, usually, chemical coagulation is followed by
algal species that were evaluated. Depending on the type of algal spe- dissolved air flotation for the purification of effluent, instead of har-
cies, the optimal centrifuge system is selected as high g-force may cause vesting microalgal biomass [12]. It was reported in a study that high
cell lysis [49]. Most large scale centrifuges operate at 5000-10,000 g- quantity of alum (0.3 g L−1) enables recovery of microalgae from pig
force and are capable of achieving 95% harvesting efficiency under slurry [58]. Although the dissolved air flotation process is an efficient
good operational conditions. The decanter type centrifuge is the op- harvesting option, it requires high pressure making the process more
timal centrifuge for the mass harvesting of microalgae biomass, as it energy-intensive [59].
doesn’t require to stop regularly and clean manually like the batch type The electro-flotation process is not considered as the optimum
centrifuges [47]. method for harvesting microalgae as the method is effective only at a
High solid fractions, along with the continuous discharge of the bench scale, and moreover, the process is an energy-intensive one like
product can be achieved through decanter type centrifuges [50]. 22% DAF [42]. Research suggested that electro-flotation process is more
of TSS is possible to obtain through decanter type centrifuge [47]. effective in marine water than freshwater [55]. Quantum Fracturing™ is
However, a study found that the decanter type centrifuge is not suitable a method developed by Origin Oil that applies pulsed electromagnetic
for Chlorella sp, which is a commonly grown and commercially im- fields and modified pH to fracture the microalgal cells and release the
portant species [50]. Moreover, the microalgal cells are exposed to high microalgal lipids to the surface and letting the remains of microalgal
shear and gravitational forces during centrifugation that may impair biomass to settle out [60].
the cell structure, resulting in loss of valuable materials. A study found The University of Sheffield applied fluidic oscillation to develop an
that for a feed rate of 1 L min−1 the energy consumed during micro- energy-efficient method for generating micro-bubbles [61]. Recently it
algae harvesting through centrifugation is 8 kW h m-3 of microalgae has been seen that micro-bubbles produced by fluidic oscillation are
suspension. However, energy consumption can be reduced by 10-fold if being able to harvest microalgal biomass from growth medium effec-
the feed rate is increased to 18 L min−1, but this will result in low tively [59]. However, more research must be carried out to make it
harvesting efficiency. Thus, the low efficiency and high flow rate cen- practically feasible to harvest large-scale microalgae through the en-
trifugation strategy was able to harvest oleaginous algae at $0.864 L−1 ergy-efficient micro-bubbles [62].
oil as opposed to $4.52 L−1 oil using numbers provided by the De- Flotation of microalgal biomass with the aid of small bubbles re-
partment of Energy for centrifugation harvesting [51]. quires high energy and operational costs. The cost involved in the flo-
Despite high operational cost and probability of cell damage owing tation process in which the flocculant needs to be added may be the
to the high shear force, centrifugation is still the most widely applied same as or greater than the cost involved during the centrifugation
harvesting technique. This is attributed to its advantageous features process [48]. Research still needs to be carried out to scale-up the low-
such as high harvesting efficiency, rapid harvesting capability, strain energy flotation techniques and make the flotation process economic-
independency and a negligible chance of contamination. The biomass ally and technically feasible.
harvested through centrifugation can be safely used for high valued Low operational costs, less space requirement, shorter operational
products. times and large-scale applicability are some of the major advantages of
the flotation process. However, high-energy consumption and species-
3.1.3. Flotation specificity are the two significant shortcomings that might hinder the
Studies found that for most of the microalgal species recovery of commercialization of the process. Various flotation methods used for
microalgal biomass through flotation is relatively fast in comparison to harvesting of microalgae is detailed in Table 2.
4
M. Roy and K. Mohanty Algal Research 44 (2019) 101683
Fig. 1. The scheme of proposal for the froth flotation harvesting of microalgae using Gemini N,N′-bis(cetyldimethyl)-1,4-butane diammonium dibromide (BCBD) or
cetyltrimethylammonium bromide (CTAB) as the collector (Adapted from Ref. [57]).
Table 2
Different flotation methods used to harvest microalgae.
Microalgae Flotation Coagulant Algal concentration Dosage pH Working Process time Harvesting Efficiency Ref.
method volume (min) (%)
C.vulgaris BBF Chitosan 7.60 ± 1.8 × 106 30 mg L−1 7.5 2L 2 92.47 [155]
cells·mL−1
Nannochloropsis sp. BF MPOE – 50,000 mg L−1 8 100 m L 120 86.5 [156]
C.vulgaris DAF C16TAB – 80 mg L−1 – 1L – 89.23 [157]
Chlorella sp. EF Chitosan – 20 mg L−1 6 200 mL 20 90 [158]
Chlorella sp. FF CTAB 126.14 ± 10.06 mg L−1 10 mg L−1 – – 30 – [159]
Dunaliella salina MF FeCl3 – 150 mg L−1 5 – – 99.2 [59]
C. vulgaris CBBF Fly ash – 2.83 g L 2.41 2L 17.05 93.04 [160]
C. vulgaris FF CTAB 0.46 ± 0.13 g L−1 35 mg L−1 – – 2 95 [161]
Tetraselmis sp. FF DPC 370 ± 36 mg L−1 15 mg L−1 9.5 35 L 15 99 [162]
C. vulgaris BDAF microspheres 7.6 ± 1.8 × 106 cells mL−1 550 mg L−1 3 1L 3 85.04 [163]
Buoy-bead flotation (BBF); Compound buoy-bead flotation (CBBF); Bio-flotation (BF); Dissolved air flotation (DAF); Electrolytic flotation (EF); Froth flotation (FF);
Microflotation (MF); Moringa protein extract-oil emulsion (MPOE); cationic cetyltrimethylammonium bromide (CTAB); Ozone flotation (OF); Ballasted dissolved air
flotation (BDAF); Dodecyl pyridinium chloride (DPC).
5
M. Roy and K. Mohanty Algal Research 44 (2019) 101683
[164]
[165]
[166]
[167]
[168]
[169]
[170]
[171]
[172]
[69]
Ref.
follows a common rule of thumb according to which a membrane fil-
tration must have pore size 10–20 times smaller than the cells that are
to be retained [20]. Research by Rossi et al. [67] found that ultra-
filtration membrane performs better than microfiltration membranes at
12.5
150
shear enhancement [70]. The PES/MWCNT-1/LiBr-5 membrane de-
86
10
–
–
–
–
–
–
veloped by thermally induced phase separation process exhibited high
porosity and hydrophilic nature, which contributed to remarkable algae
permeation and anti-fouling properties, respectively [71]. Polymeric
31,026 Pa
86.43 kPa
34.5 kPa
100 kPa
1.5 bar
and ceramic membranes are most commonly used to recover a wide
70 kPa
60 kPa
TMP
variety of microalgae, although polymeric membranes are mostly pre-
–
ferred because of their low cost.
Since membrane filtration is a chemical-free method of harvesting,
the desired product can be easily extracted from the biomass [65]. Few
Scale
Pilot
Lab
Lab
Lab
Lab
Lab
Lab
Lab
Lab
Lab
literatures have detailed about the cost involved during the process and
energy consumed is generally not determined.
Filtration is a highly efficient and chemical-free process. The cell
integrity remains undisturbed; hence, this harvesting technique is ap-
−1
− 1
is well suited for human and animal food applications. However, high
0.2 g L−1
0.5 g L−1
29 mg L
2.9 g L
operational costs due to pumping requirements and the high tendency
of membrane fouling along with low membrane selectivity are the
–
–
–
underlying weaknesses of this process. Various filtration techniques
employed for microalgal harvesting is depicted in Table 3.
Pore size/ MWCO
∼0.02 μm
0.45 μm
0.1 μm
1.2 μm
0.2 μm
0.2 μm
polyvinylidene di-fluoride
polyvinylidene di-fluoride
Polyvinylidene floride
Various microfiltration and ultrafiltration membranes used to harvest microalgae.
groups on the cell surface and tends to adsorb the ions excreted from
Membrane material
Polyvinylchloride
Polyvinylchloride
cellulose acetate
Microfiltration
Microfiltration
Microfiltration
Microfiltration
Microfiltration
Ultrafiltration
Ultrafiltration
the media and the flocculants may not be possible [23]. An ideal floc-
Arthrospira sp.
M. aeruginosa
C.zofingiensis
Chlorella sp.
Chlorella sp.
culant should: (a) not alter the quality of the biomass; (b) be eco-
Microalgae
large scale; (d) permit the reusability of the culture medium [14].
Inorganic chemicals possessing multivalent cations such as ferric
6
M. Roy and K. Mohanty Algal Research 44 (2019) 101683
chloride, ferric sulfate, and aluminum sulfate are the most widely used
[173]
[174]
[175]
[173]
[173]
[176]
[173]
[173]
[177]
[173]
[175]
[173]
[46]
[78]
Ref.
inorganic flocculants (Table 4). The addition of iron or aluminum-based
inorganic flocculants either reduces or neutralizes the negative charge
Requires high coagulant dose, risk of cell damage and contamination, pH sensitive
attributed by COOH terminal on the microalgal cell surface [31]. Dis-
Requires high coagulant dose, pH sensitive, residual iron in microalgal biomass
Risk of cell damage, requires high coagulant dose, long settling period
Flocculation efficiency of a flocculant is determined by its ionic
strength. Therefore, ferric chloride and aluminum sulfate having tri-
Microalgal biomass gets contaminated with residual aluminum
Reusability of the medium; long settling period, pH sensitive
valent cationic salts are the most widely used flocculant as compared to
Risk of cell contamination, requires high coagulant dose
82.60
66.60
≥90
≥85
≥95
98
90
95
80
90
99
66
98
180
240
10
10
10
10
30
10
10
15
10
10
–
250 mg L−1
250 mg L−1
100 mg L−1
150 mg L−1
300 mg L−1
250 mg L−1
250 mg L−1
38-120 mM
5.4 mg L−1
0.1 g L−1
30 ppm
few milligrams per litre, and they generate smaller sludge volume
without consumption of alkalinity [42]. Polymeric flocculants such as
cationic polymers possess the dual ability of coagulation and floccula-
220 × 106 cells mL−1
Algal concentration
–
–
–
–
–
[81].
In contrast to natural polymeric flocculants, synthetic organic
polymeric flocculants (e.g. Polyacrylamide and its derivatives) releases
very toxic monomers such as acrylamide and ethyleneimine, which may
Flocculant
Fe2(SO4)3
Fe2(SO4)3
Fe2(SO4)3
Fe2(SO4)3
Al2(SO4)3
Al2(SO4)3
FeCl3
FeCl3
FeCl3
NH3
PAC
Phaeodactylum tricornutum
culants such as starch, cellulose, and chitosan have received more in-
Chlorella minutissima
Scenedesmus sp.
C. sorokiniana
C. sorokiniana
Chlorella sp.
Chlorella sp.
Microalgae
S. obliquus
N. salina
high salinity of the sea and brackish waters leads to shrinking of the
polymers to a smaller size, thus, failing to bridge the algal cells [86].
7
M. Roy and K. Mohanty Algal Research 44 (2019) 101683
[177]
[178]
[175]
[179]
[180]
[180]
[180]
[181]
[180]
[182]
[181]
[183]
[142]
Ref.
incompetence of polymeric flocculants to flocculate marine microalgae
[42]. Cationic polymers are found to be effective in flocculating mi-
croalgae when the salinity of the medium is less than 5 g L−1 [75].
Non-biodegradable, carcinogenic
Cellulose modification by introducing the desired functionality is a
novel approach for increasing the flocculant efficiency. Highly cationic
Dosage-dependent
sensitive to interference by algal organic matter and was able to achieve
flocculation efficiency > 95% at a dosage of 0.1 g g−1 [88]. Recently,
biodegradable
algal harvesting via CO2-switchable 1-(3-aminopropyl)imidazole
Non-toxic
Features
chitosan
(APIm)-modified CNC was considered to be a greener and energy-effi-
cient approach as the process involved biocompatible substances such
as cellulose, CO2, and air. The CO2-switchable APIm-modified CNC
R (%)
96.5
91.8
86.5
showed strong electrostatic interaction with Chlorella vulgaris upon
90
98
98
72
90
95
88
95
95
3
CO2-treatment. Moreover, the process facilitated the reusability of re-
dispersed CNC and harvested medium for further harvesting and cul-
tivating algae, respectively [89]. Biocompatible anionic cellulose na-
Process time
nofibrils (CNF) developed from tunicate was found to be highly efficient
in harvesting microalgae and producing lipid by exploiting the size
(min)
120
15
60
60
60
30
30
30
60
30
15
effect of CNF on its geometric structure and microalgal mechan-
–
otransduction [90].
Flocculant dose
1000 mg L−1
16.5 mg L−1
40 mg L−1
60 mg L−1
70 mg L−1
30 mg L−1
60 mg L−1
10 mg L−1
20 mg L−1
34 mg L−1
35 mg L−1
20 mg L−1
16 mg L−1
efficiently with no energy input. However, its commercial application is
hampered due to the high cost of organic flocculants. Organic floccu-
lants used for harvesting microalgae along with their features are de-
tailed in Table 5.
104.62 mgdry weight L−1
665 × 106 cells ml−1
Algal concentration
0.12 g L−1
3.3.1. Autoflocculation
Autoflocculation of microalgae is defined as the ability of microalgal
–
–
–
–
cells to form flocs spontaneously. Some microalgae can also be seen to
flocculate in response to environmental stress such as pH, changes in
Tannin, quaternary ammonia
Evaluation of several organic flocculants based on their harvesting efficiencies.
nutrient content and dissolved oxygen [91]. Among all the harvesting
techniques, autoflocculation is the most inexpensive, eco-friendly
method, and the process holds good for reusing the medium [92]. A
Natural polymer
Polyacrylamide
Polyacrylamide
Polyacrylamide
Potato starch
teracts with divalent cations [94]. Calcium and phosphate ions get
supersaturated with the increase of pH, causing the neutralization of
salt
–
–
–
–
Magnafloc LT225
Nano-chitosan
Emfloc KC750
Chitosan
polymer
Scenedesmus acuminatus
obtained.
Chlorella vulgaris
C. protothecoides
Scenedesmus sp.
Muriellopsis sp.
Chlorella sp.
[92,98,99].
8
M. Roy and K. Mohanty Algal Research 44 (2019) 101683
3.3.2. Bioflocculation
[103]
[184]
[105]
[185]
[153]
[186]
[187]
[188]
[189]
[190]
Ref.
Bioflocculation is a flocculation process where microalgal cells are
flocculated with the assistance of microorganisms [100]. In this har-
Environment friendly
Economically viable
polysaccharides (EPS) secreted by microorganisms, attachment capa-
Optical density (OD); Poly γ-glutamic acid (γ-PGA); Extracellular polymeric substances (EPS); Polyethylenimine (PEI); Fungal spore-assisted (FSA); Fungal pellet-assisted (FPA).
city between microalgae and polymers and growth phase of the mi-
production
croorganisms [75]. Uronic acids and pyruvic acids are the most com-
Features
monly involved EPS during bioflocculation [102]. Charge
intact
neutralization, electrostatic patch or bridging are the mechanisms in-
volved in microbial bioflocculation, where the bioflocculants with po-
88 (pH 8.7)
95 (pH 7.5)
92.2 (pH 4-
sitively charged functional groups aggregate with the negatively
99 (pH 7)
charged microalgal cells [103].
90-93
64.86
R(%)
≥98
Flocculants extracted from microorganisms reduce the cost of har-
95
92
83
5)
vesting to a great extent by eliminating the need for chemical floccu-
Process time
lants. However, during bioflocculation, there is a chance of microbial
180 min
150 min
contamination. Hence, the microalgal biomass harvested through this
10 min
30 min
1 min
28 h
process is not safe for food applications. Microorganisms involved in
–
–
–
bioflocculation may even add on to the total lipid content [46]. Poly γ-
10 g (wet weight)
of 92% [104]. Bacillus subtilis rich in poly γ-glutamic acid
Flocculant dose
1
(19–22 mg L−1) was successful in harvesting 95% and more than 90%
0.1 mg mL−
0.1% (w/v)
2.5 mg L−1
21 mg g−1
20 mg L−1
of C. vulgaris, C. protothecoides and N. oculata LICME 002, P. tricornutum
respectively [105]. Thus, poly γ-glutamic acid facilitated biofloccula-
tion proved to be an efficient harvesting method as it does not interfere
–
with the cell integrity and the lipid content of the biomass.
Algal concentration
1 OD @660 nm
and fungi. The fungi uptakes the nutrients especially exuded poly-
20 mg·L−1
1.2 g L−1
0.5 g L−1
1.2 g L−1
saccharides produced by microalgae during the photosynthetic process,
and in return the algae is protected from the external environment by
the fungal filaments, which also holds the culture medium, thus, pro-
–
–
–
–
viding a large area for nutrients uptake [106]. The self-pelletization
process of filamentous strains can be elucidated by either coagulative or
Proteins extracted from bio-
Bioflocculant
Bioflocculant
to form aggregates. The fungal strains such as Rhizopus sp., Mucor sp.
γ-PGA
γ-PGA
FSA
EPS
PEI
pellet strains retard the spore aggregation rate and time, thereby al-
lowing the spores to germinate first and then form pellets [108,109]. It
S. bayanus var. uvarum
has been reported that Rhizopus arrhizus and Mucor rouxii spores ger-
Bacillus licheniformis
Solibacillus silvestris
Pleurotus ostreatus,
Escherichia coli
Bacillus subtilis
Desmodesmus brasiliensis
Chlorella zofingiensis
Chlorella vulgaris
Chlorella vulgaris
Chlorella sp.
Chlorella sp.
9
M. Roy and K. Mohanty Algal Research 44 (2019) 101683
Table 7
Mechanisms of microalgal cells flocculation [23,168,169].
Mechanism Description Illustration
Charge neutralization When positively charged ions, polymers or colloids strongly adsorb onto the negatively charged surface of an algal
cell, eventually canceling the negative surface charge, the phenomenon is known as charge neutralization. This results
in the loss of electrostatic repulsion between the algal cells, which consequently forces them to flocculate.
Electrostatic patching The positively charged polymer binds to the algal cell surface and locally reverses the charge on the algal surface.
Thus, algal cells attract patches of opposite charge, resulting in flocculation of the suspended algal cells.
Bridging Cationic polymers simultaneously bind to the surface of two or more algal cells, resulting in bridge formation between
the algal cells.
Sweeping Algal cells are flocculated by entrapping the cells in a massive polymeric precipitation.
3.3.3. Factors influencing microalgal flocculation such as iron or aluminum releases metal cations that induce coagulation
There are four mechanisms by which microalgal cells flocculate [42]. In the process of electro-flocculation flocculants are not required,
(Table 7). Researchers have found that characteristics of microalgal cell and the only requirement is an electricity supply [114]. In this process,
surfaces play a key role in flocculation. Moreover, these characteristics the electrodes are positioned vertically in the medium, the negatively
of cell surfaces differ among the species and vary within a species based charged microalgae move towards the positively charged anode, re-
on culture conditions. Smaller algal cells require higher flocculant do- sulting in charge neutralization and enabling to form aggregates [115].
sages to be harvested when compared to the larger cells of the same Electroflotation follows the same principle as electroflocculation in
amount because the ratio of the microalgal cell surface to biomass de- which the anode is an active metal. Recently, electro-coagulation-flo-
creases with increasing cell size [91]. Flocculation is also influenced by tation (ECF) process came to limelight as an alternative to coagulation
the varying biochemical composition of the algal cell surface [113]. The process, in which the hydrogen bubbles generated through water
pH of the growth medium plays an important role in flocculation by not electrolysis at the anode is coupled with the electrocoagulation process
only altering the charge of an algal cell surface but also of chemical at the cathode [116].
flocculants. Furthermore, a large amount of AOM consisting of proteins Electrical based harvesting technique applies two types of elec-
and polysaccharides are often excreted in the growth medium. These trodes, sacrificial and non-sacrificial [42]. In the case of sacrificial
organic matters may interact with flocculants and thus, inhibit floccu- electrodes, the metal ions are released from the active anode to the
lation of algal cells [22]. The protein excreted in the medium forms culture broth based on the current intensity of the electrolytic solution.
complexes with the cationic ions of most chemical flocculants whereas The released cationic metal ions then destabilize and aggregate the
polysaccharides interact with the cationic flocculants, thus, making the anionic microalgal cells [42]. The cationic ions that are released from
flocculants unavailable for flocculating microalgal cells. The algal the anode are not toxic as compared to chemical coagulants [117].
growth phase plays a leading role in flocculation as pH of the culture However, in the case of non-sacrificial electrode, the negatively charged
medium, dissolved carbon dioxide, zeta potential, and algal cell size microalgal cells move towards the anode. Once the microalgal cells
varies significantly throughout the growth period [75]. As these factors reach the anode, they destabilize and aggregate. The use of non-sacri-
tend to vary with the algal growth, it is difficult to obtain the optimum ficial electrodes leads to fouling. The material of the electrodes influ-
flocculant dose. The polymer dosage plays a vital role in flocculation. ences the efficiency of the electrical based harvesting process. In this
Weak polymer bridging may result if the polymer dosage is less than the harvesting process, electrodes are most commonly made of aluminum
optimum amount and the potential of bridging may be impaired due to and iron. As compared to aluminum electrodes, iron electrodes have
electrostatic hindering if the dosage is too high [75]. Therefore, among lower current efficiency due to which iron electrodes dissociate to a
all the growth phases, the stationary phase is found to be advantageous lower extent resulting in lower harvesting efficiency [75]. Moreover,
as the cellular metabolic activity, zeta potential and cell mobility is ferric electrode consumes more energy and ferric oxide formation re-
lowered, and intercellular interactions are raised [30]. Studies found sults in browning of slurry. So, the aluminum electrodes have received
that as the ionic strength of the marine water is more, so it reduces the more attention as compared to iron electrodes [75].
chemical activity of the flocculants. Hence, the marine microalgae re- Current density is inversely proportional to the harvesting period
quire more flocculant dose as compared to freshwater microalgae [42]. and plays a key role in electroflocculation. Various electroflocculation
strategies are described in Table 8. With the increase in current density,
more cationic metal ions are formed at the anode by oxidation, thus,
3.4. Electrical based harvesting techniques
improving the harvesting efficiency by decreasing the time required for
harvesting [75]. However, energy consumption increases with the
Electro-flocculation is a physicochemical process where an anode
10
M. Roy and K. Mohanty Algal Research 44 (2019) 101683
increase of current density. Gao et al. [116] found that energy con-
[116]
[116]
[191]
[192]
[193]
[194]
[195]
[196]
[197]
[198]
Ref.
sumption increased from 0.2 kWh m−3 to 2.28 kW h m−3 when the
current density was increased from 0.5 mA cm−2 to 5.0 mA cm−2.
Biomass contamination
Biomass contamination
and energy consumption [75]. Mixing and settling were carried out post
Potential to sterilize
electroflocculation to reduce energy consumption. Mixing increases the
probability of cell contact and allows the cells to aggregate [75]. On the
Not efficient
wastewater
extraction.
other hand, higher harvesting efficiency with lower settling time was
Features
83 (pH 9)
78.9 (pH
95.83
> 97
4–7)
95.4
90
95
83
36 °C [116]. An increase in process temperature also helps in reducing
the electrolysis time as it enhances the dissolution rate of metal ions
Process time
45
60
10
20
of the medium tend to affect the transport of algal cells [119]. The type
5
1
Aluminum
Aluminum
Aluminum
Aluminum
Aluminum
Electro-coagulation-flotation (ECF); Electro-flocculation (EF); Electro-Coagulation (EC); Dry weight (DW); Electrochemical harvesting (ECH).
has been observed that a high initial cell density reduces the harvesting
density/ Voltage
2.9 mA cm−2
8.3 mA cm−2
5.6 mA cm−2
efficiency, as initial cationic metal ions are not sufficient for harvesting
10 mA cm−2
1 mA cm−2
−2
the excess microalgal cells. An initial cell density of 0.55 × 109 cells
1 mA cm
L−1 required only 25 min for harvesting the cells, whereas an initial cell
4.6 V
10 A
40 V
10 V
1000
1000
600
500
900
200
90
tends to contaminate the algal slurry with the residual metals released
–
from metallic electrodes during the process. Since these trace metals
0.55 × 109–1.55 × 109 cells L−1
−1
0.55 × 10 –1.55 × 10 cells L
may impair the value of the end products, further processing may be
required [120].
9
process may impair cell integrity. There is also a high chance of cathode
106 cell ml−1
2.5 g DW
–
Flocculation type
ECF
ECF
ECF
EC
EF
EF
EF
EF
Microcystis aeruginosa
Scenedesmus obliquus
Scenedesmus obliquus
Nannochloropsis sp.
D. subspicatus
Microalgae
11
M. Roy and K. Mohanty Algal Research 44 (2019) 101683
Fig. 2. Approaches employed to promote the attachment of magnetic nanoparticles onto microalgae; (A) attached-to strategy, (B) immobilized-on strategy.
harvesting both marine and freshwater microalgal cells [121]. Among This harvesting approach is highly efficient, eco-friendly, requires
various magnetic nanoparticles, Fe3O4 particles were successfully used low energy and enables the medium along with the nanoparticles to be
for recovering a wide range of microalgal strains owing to its specific reused. However, the process requires a high dose of magnetic nano-
surface area and super-paramagnetism [124]. Researchers found that particles. These nanoparticles are expensive and require special
up to 95% of harvesting efficiencies can be obtained for freshwater equipment for recycling them. The problems mentioned above stand as
microalgal species Botryococcus braunii and Chlorella ellipsoidea, and the the major drawback of this technique. Various types of magnetic par-
marine species Nannochloropsis maritima using Fe3O4 nanoparticles ticle used for recovering microalgae are evaluated in Table 9.
synthesized through chemical co-precipitation [124,125]. Relatively
high harvesting efficiency was attained with naked iron oxide magnetic
microparticles (IOMMs), as IOMMs releases cationic Fe ions from its 4. Emerging trends in harvesting biomass
surface which acts as flocculant, thus, facilitating the harvesting process
[123]. However, the chance of biomass contamination with the re- Researchers are trying to investigate and develop energy-efficient
leased metal ions is one of the major disadvantages of this harvesting technologies to harvest microalgal biomass. Bosma et al. [132]
process [126]. exploited the dielectric properties of microalgal cells using the ultra-
As the surface charge of uncoated magnetic particles is pH-depen- sound and was successful in recovering 92% of the microalgal biomass
dent with an isoelectric point of around 7, the uncoated surface needs to in lab-scale. The high frequency generated during ultrasonic separation
be functionalized with cationic ions to enhance the harvesting effi- causes the microalgal cells to shift in the direction of the nodes of the
ciency [127]. In case of surface functionalized magnetite, there are two standing waves, resulting in flocculation and sedimentation of the
strategies for tagging polyelectrolyte, “attached-to” and “immobilized- biomass. Ultrasonic treatment not only helps in the recovery of the
on” strategy (Fig. 2). In the “attached-to” approach, the surface of mi- biomass at a high-frequency regime (1–2 MHz) but also helps to lyse the
croalgal cells is coated with a polymer binder that helps attach with the cells by cavitation and streaming at low-frequency regime (< 1 MHz)
magnetic particles. In case of “immobilized-on” strategy surface of the [132,133]. Marrone et al. [133] found this harvesting technology to be
uncoated magnetic particles are functionalized with a polyelectrolyte energy saving as compared to centrifugation. Moreover, NAABB Sus-
that aids the binding with the algal cells [128]. A higher harvesting tainability Team found that a very low amount of greenhouse gases are
efficiency was attained with an equivalent dose of particles in the emitted by ultrasonic technology [133].
“immobilized-on” approach compared to the “attached-to” approach Super absorbent polymers provide a new approach to recover the
owing to the superior distribution and colloidal stability of the “im- biomass by absorbing the water from the medium. Campo et al. [134]
mobilized-on” particles [129]. Thus, the “immobilized-on” strategy is performed research using a polyacrylic polymer ranging in diameter
widely used. from 2.0 mm to 2.5 mm. He observed that the polymer could absorb
The “immobilized-on” approach based chitosan-Fe3O4 nanoparticle water at 148 g H2O g−1 polymer allowing a volumetric concentration
composites were able to harvest 99% of Chlorella sp. KR-1 without al- factor of 60 for C. reinhardtii [134]. However, the polymer tends to get
tering the culture medium pH. Moreover, this magnetophoretic process neutralized by the medium salts, making it difficult to separate the
showed the potential for reducing the cost of algal fuel production by polymer from the biomass.
recycling the harvested medium without any adverse effects on algal Bioreactor designs, along with the cultivation strategies may play a
cell growth [130]. In another study, recyclable aminoclay-nanoscale vital role in harvesting microalgal biomass with minimal cost and ef-
zero-valent iron (nZVI) composite was able to harvest ∼100% Chlorella fort. Recently, attached cultivation technology was applied which of-
sp. KR-1 within a short time of 3 min at a > 20 g L−1 loading of the fered higher aerial biomass productivity along with real scalability
composite under an external magnetic field [125]. Similarly, BaFe12O19 prospects and this technology also saved water to a considerable extent
particles functionalized by (3-aminopropyl)triethoxysilane (APTES) [135]. A study obtained high biomass productivity along with high
harvested 99% of Chlorella sp. KR-1 and after harvesting, the detach- fatty acid yield when the microalgae cultures were grown in a thin layer
ment efficiency of BaFe12O19 particles from algae-particle conglomer- of polystyrene immobilized onto a support. In this technology, the
ates was found to increase proportionally with the size of magnetic microalgal biomass was harvested by scrapping the support, and the
particles [131]. residual colonies of microalgae on the support were reused as an in-
oculum for re-growth [136].
12
M. Roy and K. Mohanty Algal Research 44 (2019) 101683
Diethylaminoethyl magnetic beads (DEAE MBs); Magnetic-nanoparticle flocculants (dMNF- Fe3O4); Octyltriethoxysilane (OTES); Iron oxide magnetic microparticles (IOMMs); Iron oxide nanoparticles (NPs);
Genetic modification of microalgae through the expression or si-
[199]
[200]
[124]
[201]
[122]
[202]
[123]
[203]
[129]
[204]
Ref.
lencing of exogenous and endogenous genes respectively may improve
the flocculation process. Scholz et al. [137] flocculated 83 ± 3% of the
> 90 (pH
> 95 (pH
> 95 (pH
99 (pH 8) wall-deficient cells of the cw 15 mutant of Chlamydomonas reinhardtii
under alkaline conditions, whereas only 24 ± 2% of the wildtype
R (%)
98.5
96.6
strain was flocculated under the same condition. Moreover, Sapphire
99
95
99
99
2)
8)
8)
Energy described a flocculation method in which ligand-receptor pairs
can be expressed in a sequential and non-sequential manner to induce
extent.
83%
80%
–
–
1-2
10
1
–
10 mL
10 mL
5 mL
–
–
microalgae
plied for dewatering [125]. Collotta et al. [141] carried out a com-
Algal concentration
∼2 g L−1
1.6 g L−1
0.3 g L−1
lation, the results indicated that flocculation is the most suitable har-
vesting technique as it has the lowest energy demand and environ-
Uncoated Iron oxide particles
MagSilica
trifugation does not require the addition of flocculants, and so the algal
cake is digested anaerobically for energy recovery. During flocculation
Chlamydomonas reinhardtii
Chlorella vulgaris
found that 2 mg L−1 to 200 mg L−1 is the optimal chitosan loading rate
depending on the algal species. The cost of chitosan is estimated to be
13
M. Roy and K. Mohanty Algal Research 44 (2019) 101683
Table 10
LCA and TEA of various types of microalgal harvesting technologies.
Harvesting method Microalgae sp. Harvesting Energy required Estimated cost GHG (gCO2-eq Ref.
efficiency (%) MJ−1)
14
M. Roy and K. Mohanty Algal Research 44 (2019) 101683
makes the quality and quantity of the recovered biomass comparatively 10.1016/j.biortech.2013.06.010.
inferior. On the other hand, in case of biological harvesting methods, [12] L. Christenson, R. Sims, Production and harvesting of microalgae for wastewater
treatment, biofuels, and bioproducts, Biotechnol. Adv. 29 (2011) 686–702,
there is a risk of microbiological contamination and the process re- https://doi.org/10.1016/j.biotechadv.2011.05.015.
quires a high organic carbon source for cultivating the bioflocculants. [13] V. Kumar, M. Muthuraj, B. Palabhanvi, A.K. Ghoshal, D. Das, High cell density
Electrical based harvesting methods lag behind due to high operating lipid rich cultivation of a novel microalgal isolate Chlorella sorokiniana FC6 IITG
in a single-stage fed-batch mode under mixotrophic condition, Bioresour. Technol.
cost and fouling or corrosion of electrodes. Although the magneto- 170 (2014) 115–124, https://doi.org/10.1016/j.biortech.2014.07.066.
phoretic separation of microalgae is superior to traditional harvesting [14] E.M. Grima, E.-H. Belarbi, F.G.A. Fernández, A.R. Medina, Y. Chisti, Recovery of
methods, still there is a need to decrease the cost of harvesting process microalgal biomass and metabolites: process options and economics, Biotechnol.
Adv. 20 (2003) 491–515.
for the industrial-scale application. [15] L. Amer, B. Adhikari, J. Pellegrino, Technoeconomic analysis of five microalgae-
Most of the harvesting techniques were carried out in lab-scale and to-biofuels processes of varying complexity, Bioresour. Technol. 102 (2011)
therefore, outdoor compatibility of the various harvesting techniques 9350–9359, https://doi.org/10.1016/j.biortech.2011.08.010.
[16] R. Henderson, S.A. Parsons, B. Jefferson, The impact of algal properties and pre-
needs to be evaluated. Based on the above problems, either employ-
oxidation on solid–liquid separation of algae, Water Res. 42 (2008) 1827–1845,
ment of a combination of harvesting processes or alteration of genetic https://doi.org/10.1016/j.watres.2007.11.039.
properties through genetic engineering would be the best solution to [17] J.F. Sánchez, J.M. Fernández-Sevilla, F.G. Acién, M.C. Cerón, J. Pérez-Parra,
attain enhanced harvesting efficiency at reduced operational costs. E. Molina-Grima, Biomass and lutein productivity of Scenedesmus almeriensis:
influence of irradiance, dilution rate and temperature, Appl. Microbiol.
Commercially potential microalgal species can be genetically en- Biotechnol. 79 (2008) 719–729, https://doi.org/10.1007/s00253-008-1494-2.
gineered for enhanced autoflocculation via recombinant DNA tech- [18] G.O. James, C.H. Hocart, W. Hillier, G.D. Price, M.A. Djordjevic, Temperature
nology. This can be accomplished by identifying the gene responsible modulation of fatty acid profiles for biofuel production in nitrogen deprived
Chlamydomonas reinhardtii, Bioresour. Technol. 127 (2013) 441–447, https://
for autoflocculation in some specific microalgal species and tailoring doi.org/10.1016/j.biortech.2012.09.090.
them into a desired algal species via modern genetic tools. Ongoing [19] M.L. Gerardo, S. Van Den Hende, H. Vervaeren, T. Coward, S.C. Skill, Harvesting
research should aim to develop an economically sustainable harvesting of microalgae within a biorefinery approach: a review of the developments and
case studies from pilot-plants, Algal Res. 11 (2015) 248–262, https://doi.org/10.
process based on the physical properties of microalgae, the chemical 1016/j.algal.2015.06.019.
composition of culture medium and quality of the end product. At the [20] M.L. Gerardo, S. Van Den Hende, H. Vervaeren, T. Coward, S.C. Skill, Harvesting
current stage, a leap of faith is required for developing a sustainable of microalgae within a biorefinery approach: a review of the developments and
case studies from pilot-plants, Algal Res. 11 (2015) 248–262, https://doi.org/10.
harvesting method. 1016/j.algal.2015.06.019.
[21] H.C. Greenwell, L.M.L. Laurens, R.J. Shields, R.W. Lovitt, K.J. Flynn, Placing mi-
Statement of informed consent, human/animal rights croalgae on the biofuels priority list: a review of the technological challenges, J. R.
Soc. Interface 7 (2010), https://doi.org/10.1098/rsif.2009.0322.
[22] X. Zhang, P. Amendola, J.C. Hewson, M. Sommerfeld, Q. Hu, Influence of growth
No conflicts, informed consent, human or animal rights applicable. phase on harvesting of Chlorella zofingiensis by dissolved air flotation, Bioresour.
Declaration of Competing Interest Technol. 116 (2012) 477–484.
There is no conflict of interest to declare. [23] D. Vandamme, I. Foubert, K. Muylaert, Flocculation as a low-cost method for
harvesting microalgae for bulk biomass production, Trends Biotechnol. 31 (2013)
233–239, https://doi.org/10.1016/j.tibtech.2012.12.005.
Acknowledgment [24] R. Beckett, N.P. Le, The role or organic matter and ionic composition in de-
termining the surface charge of suspended particles in natural waters, Colloids
Surf. 44 (1990) 35–49.
The research was financially supported by the Ministry of Human [25] A. Paralkar, J.K. Edzwald, Effect of ozone on EOM and coagulation, Am. Water
Resource Development (MHRD), Government of India, through its Work. Assoc. J. 88 (1996) 143.
IMPRINT-1 initiative (Grant No. 7698). [26] D. Kaplan, D. Christiaen, S. Arad, Binding of heavy metals by algal poly-
saccharides, Algal Biotechnol. (1988) by T. Stadler…[et al.].
[27] J.E. Gregor, E. Fenton, G. Brokenshire, P. Van Den Brink, B. O’sullivan,
References Interactions of calcium and aluminium ions with alginate, Water Res. 30 (1996)
1319–1324.
[28] L. Brennan, P. Owende, Biofuels from microalgae-a review of technologies for
[1] J.J. Creasey, A. Chieregato, J.C. Manayil, C.M.A. Parlett, K. Wilson, A.F. Lee,
production, processing, and extractions of biofuels and co-products, Renew.
Alkali- and nitrate-free synthesis of highly active Mg–Al hydrotalcite-coated alu-
Sustain. Energy Rev. 14 (2010), https://doi.org/10.1016/j.rser.2009.10.009.
mina for FAME production, Catal. Sci. Technol. 4 (2014) 861–870, https://doi.
[29] F. Fasaei, J.H. Bitter, P.M. Slegers, A.J.B. van Boxtel, Techno-economic evaluation
org/10.1039/C3CY00902E.
of microalgae harvesting and dewatering systems, Algal Res. 31 (2018) 347–362,
[2] H. Balat, Prospects of biofuels for a sustainable energy future: a critical assess-
https://doi.org/10.1016/j.algal.2017.11.038.
ment, Energy Educ, Sci. Technol. Part A-Energy Sci. Res. 24 (2010) 85–111.
[30] M.K. Danquah, L. Ang, N. Uduman, N. Moheimani, G.M. Forde, Dewatering of
[3] S. Hemaiswarya, R. Raja, I.S. Carvalho, R. Ravikumar, V. Zambare, D. Barh, An
microalgal culture for biodiesel production: exploring polymer flocculation and
Indian scenario on renewable and sustainable energy sources with emphasis on
tangential flow filtration, J. Chem. Technol. Biotechnol. 84 (2009) 1078–1083.
algae, Appl. Microbiol. Biotechnol. 96 (2012) 1125–1135, https://doi.org/10.
[31] C.Y. Chen, K.L. Yeh, R. Aisyah, D.J. Lee, J.S. Chang, Cultivation, photobioreactor
1007/s00253-012-4487-0.
design and harvesting of microalgae for biodiesel production: a critical review,
[4] A.H. Demirbas, Inexpensive oil and fats feedstocks for production of biodiesel,
Bioresour. Technol. 102 (2011) 71–81, https://doi.org/10.1016/j.biortech.2010.
Energy Educ. Sci. Technol. Part A-Energy Sci. Res. 23 (2009) 1–13.
06.159.
[5] S. Mishra, K. Mohanty, Comprehensive characterization of microalgal isolates and
[32] J.J. Milledge, S. Heaven, A review of the harvesting of micro-algae for biofuel
lipid-extracted biomass as zero-waste bioenergy feedstock: an integrated bior-
production, Rev. Environ. Sci. Biotechnol. 12 (2013) 165–178, https://doi.org/10.
emediation and biorefinery approach, Bioresour. Technol. 273 (2019) 177–184,
1007/s11157-012-9301-z.
https://doi.org/10.1016/j.biortech.2018.11.012.
[33] F.J. Millero, F.K. Lepple, The density and expansibility of artificial seawater so-
[6] C.M. Monteiro, P.M.L. Castro, F.X. Malcata, Metal uptake by microalgae: under-
lutions from 0 to 40°C and 0 to 21‰ chlorinity, Mar. Chem. 1 (1973) 89–104,
lying mechanisms and practical applications, Biotechnol. Prog. 28 (2012)
https://doi.org/10.1016/0304-4203(73)90009-1.
299–311.
[34] T.J. SMAYDA, The suspension and sinking of phytoplankton in the sea, Oceanogr.
[7] M.A. Borowitzka, High-value products from microalgae—their development and
Mar. Biol. Ann. Rev. 8 (1970) 353–414.
commercialisation, J. Appl. Phycol. 25 (2013) 743–756.
[35] E.T. Van Ierland, L. Peperzak, Separation of marine seston and density determi-
[8] R. Raja, S. Hemaiswarya, R. Rengasamy, Exploitation of Dunaliella for $β$-car-
nation of marine diatoms by density gradient centrifugation, J. Plankton Res. 6
otene production, Appl. Microbiol. Biotechnol. 74 (2007) 517–523, https://doi.
(1984) 29–44.
org/10.1007/s00253-006-0777-8.
[36] T.M. Cole, E.M. Buchak, CE-QUAL-W2: A Two-dimensional, Laterally Averaged
[9] R. Vazhappilly, F. Chen, Eicosapentaenoic acid and docosahexaenoic acid pro-
Hydrodynamic and Water Quality Model, Version 2.0, Draft User Manual,
duction potential of microalgae and their heterotrophic growth, J. Am. Oil Chem.
Instruction Report EL-95-1, Corps of Engineers Waterways Experiment Station,
Soc. 75 (1998) 393–397, https://doi.org/10.1007/s11746-998-0057-0.
Vicksburg, MS, 1995.
[10] M. Olaizola, Commercial production of astaxanthin from Haematococcus pluvialis
[37] C.S. Reynolds, The Ecology of Freshwater Phytoplankton, Cambridge University
using 25,000-liter outdoor photobioreactors, J. Appl. Phycol. 12 (2000) 499–506,
Press, 1984.
https://doi.org/10.1023/A:1008159127672.
[38] L. Peperzak, F. Colijn, R. Koeman, W.W.C. Gieskes, J.C.A. Joordens,
[11] S. Basu, A.S. Roy, K. Mohanty, A.K. Ghoshal, Enhanced CO2 sequestration by a
Phytoplankton sinking rates in the Rhine region of freshwater influence, J.
novel microalga: scenedesmus obliquus SA1 isolated from bio-diversity hotspot
Plankton Res. 25 (2003) 365–383, https://doi.org/10.1093/plankt/25.4.365.
region of Assam, India, Bioresour. Technol. 143 (2013) 369–377, https://doi.org/
[39] S.K. Choi, J.Y. Lee, D.Y. Kwon, K.J. Cho, Settling characteristics of problem algae
15
M. Roy and K. Mohanty Algal Research 44 (2019) 101683
in the water treatment process, Water Sci. Technol. 53 (2006) 113–119, https:// harvest microalgae for biofuel, Bioresour. Technol. 119 (2012) 406–418, https://
doi.org/10.2166/wst.2006.214. doi.org/10.1016/j.biortech.2012.05.044.
[40] A.M. Waite, P.A. Thompson, P.J. Harrison, Does energy control the sinking rates of [71] N.F.M. Khairuddin, A. Idris, L.W. Hock, Harvesting nannochloropsis sp. using PES/
marine diatoms? Limnol. Oceanogr. 37 (1992) 468–477, https://doi.org/10.4319/ MWCNT/LiBr membrane with good antifouling properties, Sep. Purif. Technol.
lo.1992.37.3.0468. 212 (2019) 1–11, https://doi.org/10.1016/j.seppur.2018.11.013.
[41] P.K. Bienfang, Sinking rates of heterogeneous, temperate phytoplankton popula- [72] C.-Y. Chen, K.-L. Yeh, R. Aisyah, D.-J. Lee, J.-S. Chang, Cultivation, photo-
tions, J. Plankton Res. 3 (1981) 235–253, https://doi.org/10.1093/plankt/3.2. bioreactor design and harvesting of microalgae for biodiesel production: a critical
235. review, Bioresour. Technol. 102 (2011) 71–81.
[42] N. Uduman, Y. Qi, M.K. Danquah, G.M. Forde, A. Hoadley, Dewatering of mi- [73] I. Rawat, R.R. Kumar, T. Mutanda, F. Bux, Dual role of microalgae: phycor-
croalgal cultures: a major bottleneck to algae-based fuels, J. Renew. Sustain. emediation of domestic wastewater and biomass production for sustainable bio-
Energy 2 (2010) 12701. fuels production, Appl. Energy 88 (2011) 3411–3424, https://doi.org/10.1016/j.
[43] P. Collet, A. Hélias, L. Lardon, M. Ras, R.-A. Goy, J.-P. Steyer, Life-cycle assess- apenergy.2010.11.025.
ment of microalgae culture coupled to biogas production, Bioresour. Technol. 102 [74] N. Pragya, K.K. Pandey, P.K. Sahoo, A review on harvesting, oil extraction and
(2011) 207–214, https://doi.org/10.1016/j.biortech.2010.06.154. biofuels production technologies from microalgae, Renew. Sustain. Energy Rev. 24
[44] A. Singh, P.S. Nigam, J.D. Murphy, Renewable fuels from algae: an answer to (2013) 159–171.
debatable land based fuels, Bioresour. Technol. 102 (2011) 10–16. [75] A.I. Barros, A.L. Gonçalves, M. Simões, J.C.M. Pires, Harvesting techniques applied
[45] S. Van Den Hende, H. Vervaeren, S. Desmet, N. Boon, Bioflocculation of micro- to microalgae: a review, Renew. Sustain. Energy Rev. 41 (2015) 1489–1500,
algae and bacteria combined with flue gas to improve sewage treatment, N. https://doi.org/10.1016/j.rser.2014.09.037.
Biotechnol. 29 (2011) 23–31, https://doi.org/10.1016/j.nbt.2011.04.009. [76] T.M. Mata, A.A. Martins, N.S. Caetano, Microalgae for biodiesel production and
[46] F. Chen, Z. Liu, D. Li, C. Liu, P. Zheng, S. Chen, Using ammonia for algae har- other applications: a review, Renew. Sustain. Energy Rev. 14 (2010), https://doi.
vesting and as nutrient in subsequent cultures, Bioresour. Technol. 121 (2012) org/10.1016/j.rser.2009.07.020.
298–303. [77] J. Benemann, B. Koopman, J. Weissman, D. Eisenberg, R. Goebel, Development of
[47] G. Shelef, A. Sukenik, M. Green, Microalgae Harvesting and Processing: A microalgae harvesting and high-rate pond technologies in California, algae bio-
Literature Review, Technion Research and Development Foundation Ltd., Haifa mass prod. use/[Sponsored by Natl. Counc. Res. Dev. Isr. Gesellschaft Fur
(Israel), 1984. Strahlen-Und Umweltforsch. (GSF), Munich, Ger. Ed. Gedaliah Shelef], Carl J.
[48] F.H. Mohn, Harvesting of micro-algal biomass, Micro-Algal Biotechnol. (1988) Soeder (1980).
395–414. [78] A. Papazi, P. Makridis, P. Divanach, Harvesting Chlorella minutissima using cell
[49] M. Heasman, J. Diemar, W. O’connor, T. Sushames, L. Foulkes, Development of coagulants, J. Appl. Phycol. 22 (2010) 349–355, https://doi.org/10.1007/s10811-
extended shelf‐life microalgae concentrate diets harvested by centrifugation for 009-9465-2.
bivalve molluscs–a summary, Aquac. Res. 31 (2000) 637–659. [79] N. Rashid, M.S.U. Rehman, M. Sadiq, T. Mahmood, J.-I. Han, Current status, issues
[50] E.W. Becker, Microalgae: Biotechnology and Microbiology, Cambridge University and developments in microalgae derived biodiesel production, Renew. Sustain.
Press, 1994. Energy Rev. 40 (2014) 760–778, https://doi.org/10.1016/j.rser.2014.07.104.
[51] A.J. Dassey, C.S. Theegala, Harvesting economics and strategies using cen- [80] Z. Wu, Y. Zhu, W. Huang, C. Zhang, T. Li, Y. Zhang, A. Li, Evaluation of floccu-
trifugation for cost effective separation of microalgae cells for biodiesel applica- lation induced by pH increase for harvesting microalgae and reuse of flocculated
tions, Bioresour. Technol. 128 (2013) 241–245. medium, Bioresour. Technol. 110 (2012) 496–502, https://doi.org/10.1016/j.
[52] A. Singh, P.S. Nigam, J.D. Murphy, Mechanism and challenges in commerciali- biortech.2012.01.101.
sation of algal biofuels, Bioresour. Technol. 102 (2011) 26–34, https://doi.org/10. [81] C.S. Lee, J. Robinson, M.F. Chong, A review on application of flocculants in
1016/j.biortech.2010.06.057. wastewater treatment, Process Saf. Environ. Prot. 92 (2014) 489–508, https://doi.
[53] J.K. Edzwald, Algae, bubbles, coagulants, and dissolved air flotation, Water Sci. org/10.1016/j.psep.2014.04.010.
Technol. 27 (1993). [82] V.H. Dao, N.R. Cameron, K. Saito, Synthesis{,} properties and performance of
[54] G. Shelef, A. Sukenik, M. Green, Separation and harvesting of marine microalgal organic polymers employed in flocculation applications, Polym. Chem. 7 (2016)
biomass, Algal Biomass Technol. J. Cramer Color (1984). 11–25, https://doi.org/10.1039/C5PY01572C.
[55] W.J. Oswald, Large-scale algal culture systems (engineering aspects), Micro-Algal [83] F. Roselet, D. Vandamme, M. Roselet, K. Muylaert, P.C. Abreu, Effects of pH,
Biotechnol. (1988) 357–394. salinity, biomass concentration, and algal organic matter on flocculant efficiency
[56] Z. Huang, C. Cheng, L. Li, Z. Guo, G. He, X. Yu, R. Liu, H. Han, L. Deng, W. Fu, of synthetic versus natural polymers for harvesting microalgae biomass, Bioenergy
Morpholine-based gemini surfactant: synthesis and its application for reverse froth Res. 10 (2017) 427–437, https://doi.org/10.1007/s12155-016-9806-3.
flotation of carnallite ore in potassium fertilizer production, J. Agric. Food Chem. [84] K. Sievänen, J. Kavakka, P. Hirsilä, P. Vainio, K. Karisalmi, J. Fiskari,
66 (2018) 13126–13132, https://doi.org/10.1021/acs.jafc.8b05560. I. Kilpeläinen, Cationic cellulose betainate for wastewater treatment, Cellulose 22
[57] Z. Huang, C. Cheng, Z. Liu, W. Luo, H. Zhong, G. He, C. Liang, L. Li, L. Deng, W. Fu, (2015) 1861–1872, https://doi.org/10.1007/s10570-015-0578-2.
Gemini surfactant: a novel flotation collector for harvesting of microalgae by froth [85] N. Kumar, C. Banerjee, N. Kumar, S. Jagadevan, A novel non-starch based cationic
flotation, Bioresour. Technol. 275 (2019) 421–424, https://doi.org/10.1016/j. polymer as flocculant for harvesting microalgae, Bioresour. Technol. 271 (2019)
biortech.2018.12.106. 383–390, https://doi.org/10.1016/j.biortech.2018.09.073.
[58] A. Goh, University of Colorado, Boulder, USA, 5–7 Apr. 1984Production of [86] A. Schlesinger, D. Eisenstadt, A. Bar-Gil, H. Carmely, S. Einbinder, J. Gressel,
Microalgae Using Pig Waste as a Substrate: Presented… at Algal Biomass Inexpensive non-toxic flocculation of microalgae contradicts theories; overcoming
Workshop1984, Production of Microalgae Using Pig Waste as a Substrate: a major hurdle to bulk algal production, Biotechnol. Adv. 30 (2012) 1023–1030,
Presented… at Algal Biomass Workshop (1984). https://doi.org/10.1016/j.biotechadv.2012.01.011.
[59] J. Hanotu, H.C. Bandulasena, W.B. Zimmerman, Microflotation performance for [87] K. Muylaert, D. Vandamme, B. Meesschaert, I. Foubert, Flocculation of microalgae
algal separation, Biotechnol. Bioeng. 109 (2012) 1663–1673. using cationic starch, in: phycologia, Int. Phycol. soc. (2009) 63.
[60] G. Luísa, SpringerBriefs in Microbiology, (2011), https://doi.org/10.1007/978-3- [88] D. Vandamme, S. Eyley, G. Van den Mooter, K. Muylaert, W. Thielemans, Highly
642-17997-6. charged cellulose-based nanocrystals as flocculants for harvesting Chlorella vul-
[61] W.B. Zimmerman, B.N. Hewakandamby, V. Tesař, H.C.H. Bandulasena, garis, Bioresour. Technol. 194 (2015) 270–275.
O.A. Omotowa, On the design and simulation of an airlift loop bioreactor with [89] S. Ge, P. Champagne, H. Wang, P.G. Jessop, M.F. Cunningham, Microalgae re-
microbubble generation by fluidic oscillation, Food Bioprod. Process. 87 (2009) covery from water for biofuel production using CO2-switchable crystalline nano-
215–227, https://doi.org/10.1016/j.fbp.2009.03.006. cellulose, Environ. Sci. Technol. 50 (2016) 7896–7903.
[62] J.J. Milledge, S. Heaven, A review of the harvesting of micro-algae for biofuel [90] S. Il Yu, S.K. Min, H.S. Shin, Nanocellulose size regulates microalgal flocculation
production, Rev. Environ. Sci. Biotechnol. 12 (2013) 165–178, https://doi.org/10. and lipid metabolism, Sci. Rep. 6 (2016) 35684.
1007/s11157-012-9301-z. [91] P.M. Schenk, S.R. Thomas-Hall, E. Stephens, U.C. Marx, J.H. Mussgnug, C. Posten,
[63] M. Cheryan, Ultrafiltration and Microfiltration Handbook, Technomic Publ. Co., O. Kruse, B. Hankamer, Second generation biofuels: high-efficiency microalgae for
Urbana, Illinois, USA, 1998, pp. 245–267 (n.d.). biodiesel production, Bioenergy Res. 1 (2008) 20–43, https://doi.org/10.1007/
[64] J.F. Richardson, J.M. Coulson, Chemical Engineering: Particle Technology and s12155-008-9008-8.
Seraration Processes, Elsevier Engineering Information, Incorporated, 2002. [92] J.-I. Horiuchi, I. Ohba, K. Tada, M. Kobayashi, T. Kanno, M. Kishimoto, Effective
[65] M.L. Gerardo, D.L. Oatley-Radcliffe, R.W. Lovitt, Integration of membrane tech- cell harvesting of the halotolerant microalga Dunaliella tertiolecta with pH con-
nology in microalgae biorefineries, J. Memb. Sci. 464 (2014) 86–99. trol, J. Biosci. Bioeng. 95 (2003) 412–415, https://doi.org/10.1016/S1389-
[66] S. Zou, Y. Gu, D. Xiao, C.Y. Tang, The role of physical and chemical parameters on 1723(03)80078-6.
forward osmosis membrane fouling during algae separation, J. Memb. Sci. 366 [93] K. Spilling, J. Seppälä, T. Tamminen, Inducing autoflocculation in the diatom
(2011) 356–362. Phaeodactylum tricornutum through CO2 regulation, J. Appl. Phycol. 23 (2011)
[67] N. Rossi, P. Jaouen, P. Legentilhomme, I. Petit, Harvesting of cyanobacterium 959–966.
Arthrospira platensis using organic filtration membranes, Food Bioprod. Process. [94] R. Munoz, B. Guieysse, Algal–bacterial processes for the treatment of hazardous
82 (2004) 244–250. contaminants: a review, Water Res. 40 (2006) 2799–2815.
[68] R. Bhave, T. Kuritz, L. Powell, D. Adcock, Membrane-based energy efficient de- [95] A. Sukenik, G. Shelef, Algal autoflocculation—verification and proposed me-
watering of microalgae in biofuels production and recovery of value added co- chanism, Biotechnol. Bioeng. 26 (1984), https://doi.org/10.1002/bit.260260206.
products, Environ. Sci. Technol. 46 (2012) 5599–5606. [96] Y. Nurdogan, W.J. Oswald, Enhanced nutrient removal in high-rate ponds, Water
[69] X. Zhang, Q. Hu, M. Sommerfeld, E. Puruhito, Y. Chen, Harvesting algal biomass Sci. Technol. 31 (1995) 33–43, https://doi.org/10.1016/0273-1223(95)00490-E.
for biofuels using ultrafiltration membranes, Bioresour. Technol. 101 (2010) [97] R.M. Knuckey, M.R. Brown, R. Robert, D.M.F. Frampton, Production of microalgal
5297–5304. concentrates by flocculation and their assessment as aquaculture feeds, Aquac.
[70] S.D. Ríos, J. Salvadó, X. Farriol, C. Torras, Antifouling microfiltration strategies to Eng. 35 (2006), https://doi.org/10.1016/j.aquaeng.2006.04.001.
16
M. Roy and K. Mohanty Algal Research 44 (2019) 101683
[98] S. Salim, M.H. Vermuë, R.H. Wijffels, Ratio between autoflocculating and target [126] S.-K. Wang, A.R. Stiles, C. Guo, C.-Z. Liu, Harvesting microalgae by magnetic se-
microalgae affects the energy-efficient harvesting by bio-flocculation, Bioresour. paration: a review, Algal Res. 9 (2015) 178–185, https://doi.org/10.1016/j.algal.
Technol. 118 (2012) 49–55, https://doi.org/10.1016/j.biortech.2012.05.007. 2015.03.005.
[99] S. Koley, S. Prasad, S.K. Bagchi, N. Mallick, Development of a harvesting technique [127] A.E. Regazzoni, G.A. Urrutia, M.A. Blesa, A.J.G. Maroto, Some observations on the
for large-scale microalgal harvesting for biodiesel production, RSC Adv. 7 (2017) composition and morphology of synthetic magnetites obtained by different routes,
7227–7237, https://doi.org/10.1039/C6RA27286J. J. Inorg. Nucl. Chem. 43 (1981) 1489–1493, https://doi.org/10.1016/0022-
[100] J. Lee, D.-H. Cho, R. Ramanan, B.-H. Kim, H.-M. Oh, H.-S. Kim, Microalgae-as- 1902(81)80322-3.
sociated bacteria play a key role in the flocculation of Chlorella vulgaris, [128] P.Y. Toh, B.W. Ng, C.H. Chong, A.L. Ahmad, J.-W. Yang, C.J. Chieh Derek, J. Lim,
Bioresour. Technol. 131 (2013) 195–201. Magnetophoretic separation of microalgae: the role of nanoparticles and polymer
[101] J.A. Gerde, T. Wang, L. Yao, S. Jung, L.A. Johnson, B. Lamsal, Optimizing protein binder in harvesting biofuel, RSC Adv. 4 (2014) 4114–4121, https://doi.org/10.
isolation from defatted and non-defatted Nannochloropsis microalgae biomass, 1039/C3RA46298F.
Algal Res. 2 (2013) 145–153. [129] L.J. Kang, C.D.C. Juinn, S.A. Jalak, T.P. Yi, Y.N.H. Mat, N.B. Wah, A.A. Latif, Rapid
[102] B. Frølund, R. Palmgren, K. Keiding, P.H. Nielsen, Extraction of extracellular magnetophoretic separation of microalgae, Small 8 (2002) 1683–1692, https://
polymers from activated sludge using a cation exchange resin, Water Res. 30 doi.org/10.1002/smll.201102400.
(1996) 1749–1758, https://doi.org/10.1016/0043-1354(95)00323-1. [130] K. Lee, S.Y. Lee, J.-G. Na, S.G. Jeon, R. Praveenkumar, D.-M. Kim, W.-S. Chang, Y.-
[103] C. Wan, X.-Q. Zhao, S.-L. Guo, M.A. Alam, F.-W. Bai, Bioflocculant production K. Oh, Magnetophoretic harvesting of oleaginous Chlorella sp. by using bio-
from Solibacillus silvestris W01 and its application in cost-effective harvest of compatible chitosan/magnetic nanoparticle composites, Bioresour. Technol. 149
marine microalga Nannochloropsis oceanica by flocculation, Bioresour. Technol. (2013) 575–578, https://doi.org/10.1016/j.biortech.2013.09.074.
135 (2013) 207–212, https://doi.org/10.1016/j.biortech.2012.10.004. [131] J.Y. Seo, K. Lee, S.Y. Lee, S.G. Jeon, J.-G. Na, Y.-K. Oh, S. Bin Park, Effect of
[104] T. Ndikubwimana, X. Zeng, Y. Liu, J.-S. Chang, Y. Lu, Harvesting of microalgae barium ferrite particle size on detachment efficiency in magnetophoretic har-
Desmodesmus sp. F51 by bioflocculation with bacterial bioflocculant, Algal Res. 6 vesting of oleaginous Chlorella sp, Bioresour. Technol. 152 (2014) 562–566,
(2014) 186–193, https://doi.org/10.1016/j.algal.2014.09.004. https://doi.org/10.1016/j.biortech.2013.11.064.
[105] H. Zheng, Z. Gao, J. Yin, X. Tang, X. Ji, H. Huang, Harvesting of microalgae by [132] R. Bosma, W.A. Van Spronsen, J. Tramper, R.H. Wijffels, Ultrasound, a new se-
flocculation with poly (γ-glutamic acid), Bioresour. Technol. 112 (2012) 212–220, paration technique to harvest microalgae, J. Appl. Phycol. 15 (2003), https://doi.
https://doi.org/10.1016/j.biortech.2012.02.086. org/10.1023/A:1023807011027.
[106] W. Zhou, Y. Cheng, Y. Li, Y. Wan, Y. Liu, X. Lin, R. Ruan, Novel fungal pelleti- [133] B.L. Marrone, R.E. Lacey, D.B. Anderson, J. Bonner, J. Coons, T. Dale,
zation-assisted technology for algae harvesting and wastewater treatment, Appl. C.M. Downes, S. Fernando, C. Fuller, B. Goodall, J.E. Holladay, K. Kadam, D. Kalb,
Biochem. Biotechnol. 167 (2012) 214–228, https://doi.org/10.1007/s12010-012- W. Liu, J.B. Mott, Z. Nikolov, K.L. Ogden, R.T. Sayre, B.G. Trewyn, J.A. Olivares,
9667-y. Review of the harvesting and extraction program within the National Alliance for
[107] S.O. Gultom, B. Hu, Review of microalgae harvesting via co-pelletization with Advanced Biofuels and Bioproducts, Algal Res. 33 (2018) 470–485, https://doi.
filamentous fungus, Energies 6 (2013) 5921–5939, https://doi.org/10.3390/ org/10.1016/j.algal.2017.07.015.
en6115921. [134] J.S. Martín del Campo, R. Patiño, Harvesting microalgae cultures with super-
[108] O.M.H. de Vries, M.P. Fekkes, H.A.B. Wösten, J.G.H. Wessels, Insoluble hydro- absorbent polymers: desulfurization of Chlamydomonas reinhardtii for hydrogen
phobin complexes in the walls of Schizophyllum commune and other filamentous production, Biotechnol. Bioeng. 110 (2013) 3227–3234, https://doi.org/10.1002/
fungi, Arch. Microbiol. 159 (1993) 330–335, https://doi.org/10.1007/ bit.24989.
BF00290915. [135] O. Giuseppe, S. Piero, M. Antonio, Advances in photobioreactors for intensive
[109] A.P.J. Trinci, A study of the kinetics of hyphal extension and branch initiation of microalgal production: configurations, operating strategies and applications, J.
fungal mycelia, Microbiology 81 (1974) 225–236. Chem. Technol. Biotechnol. 89 (2014) 178–195, https://doi.org/10.1002/jctb.
[110] P.-J. Lin, L.H. Grimm, M. Wulkow, D.C. Hempel, R. Krull, Population balance 4218.
modeling of the conidial aggregation of Aspergillus niger, Biotechnol. Bioeng. 99 [136] M.B. Johnson, Z. Wen, Development of an attached microalgal growth system for
(2008) 341–350, https://doi.org/10.1002/bit.21569. biofuel production, Appl. Microbiol. Biotechnol. 85 (2010) 525–534.
[111] M.C. Morrin, Relationship Between Mycelial Morphology, Cell Wall Composition [137] M. Scholz, T. Hoshino, D. Johnson, M.R. Riley, J. Cuello, Flocculation of wall-
and Product Formation of Rhizopus Arrhizus, (1989). deficient cells of Chlamydomonas reinhardtii mutant cw15 by calcium and me-
[112] S. Bartnicki-Garcia, N. Nelson, E. Cota-Robles, Electron microscopy of spore ger- thanol, Biomass Bioenergy 35 (2011) 4835–4840, https://doi.org/10.1016/j.
mination and cell wall formation in Mucor rouxii, Arch. Mikrobiol. 63 (1968) biombioe.2011.08.020.
242–255. [138] M. Mendez, C. Behnke, Y. Poon, P. Lee, Induction of Flocculation in
[113] R.K. Henderson, A. Baker, S.A. Parsons, B. Jefferson, Characterisation of algogenic Photosynthetic Organisms, (2015).
organic matter extracted from cyanobacteria, green algae and diatoms, Water Res. [139] K. Sander, G.S. Murthy, Life cycle analysis of algae biodiesel, Int. J. Life Cycle
42 (2008) 3435–3445, https://doi.org/10.1016/j.watres.2007.10.032. Assess. 15 (2010) 704–714, https://doi.org/10.1007/s11367-010-0194-1.
[114] A.K. Patel, C. Laroche, A. Marcati, A.V. Ursu, S. Jubeau, L. Marchal, E. Petit, [140] P.M. Foley, E.S. Beach, J.B. Zimmerman, Algae as a source of renewable chemi-
G. Djelveh, P. Michaud, Separation and fractionation of exopolysaccharides from cals: opportunities and challenges, Green Chem. 13 (2011) 1399–1405, https://
Porphyridium cruentum, Bioresour. Technol. 145 (2013) 345–350. doi.org/10.1039/C1GC00015B.
[115] E. Poelman, N. De Pauw, B. Jeurissen, Potential of electrolytic flocculation for [141] M. Collotta, P. Champagne, W. Mabee, G. Tomasoni, G.B. Leite, L. Busi, M. Alberti,
recovery of micro-algae, Resour. Conserv. Recycl. 19 (1997), https://doi.org/10. Comparative LCA of flocculation for the harvesting of microalgae for biofuels
1016/S0921-3449(96)01156-1. production, Procedia CIRP 61 (2017) 756–760, https://doi.org/10.1016/j.procir.
[116] S. Gao, J. Yang, J. Tian, F. Ma, G. Tu, M. Du, Electro-coagulation–flotation process 2016.11.146.
for algae removal, J. Hazard. Mater. 177 (2010) 336–343, https://doi.org/10. [142] M.R. Granados, F.G. Acien, C. Gomez, J.M. Fernandez-Sevilla, E. Molina Grima,
1016/j.jhazmat.2009.12.037. Evaluation of flocculants for the recovery of freshwater microalgae, Bioresour.
[117] A. Zenouzi, B. Ghobadian, M.A. Hejazi, P. Rahnemoon, Harvesting of microalgae Technol. 118 (2012) 102–110, https://doi.org/10.1016/j.biortech.2012.05.018.
Dunaliella salina using electroflocculation, J. Agric. Sci. Technol. 15 (2013), [143] S.J. Lee, S.-B. Kim, J.-E. Kim, G.-S. Kwon, B.-D. Yoon, H.-M. Oh, Effects of har-
http://journals.modares.ac.ir/article-23-4125-en.html. vesting method and growth stage on the flocculation of the green alga
[118] A.K. Lee, D.M. Lewis, P.J. Ashman, Harvesting of marine microalgae by electro- Botryococcus braunii, Lett. Appl. Microbiol. 27 (1998), https://doi.org/10.1046/j.
flocculation: the energetics, plant design, and economics, Appl. Energy 108 (2013) 1472-765X.1998.00375.x.
45–53, https://doi.org/10.1016/j.apenergy.2013.03.003. [144] R. Davis, J. Markham, C. Kinchin, N. Grundl, E.C.D. Tan, D. Humbird, Process
[119] K.-Y. Show, D.-J. Lee, Chapter 5 - algal biomass harvesting, in: A. Pandey, D.- Design and Economics for the Production of Algal Biomass: Algal Biomass
J. Lee, Y. Chisti, C.R. Soccol (Eds.), Biofuels from Algae, Elsevier, Amsterdam, Production in Open Pond Systems and Processing Through Dewatering for
2014, pp. 85–110, , https://doi.org/10.1016/B978-0-444-59558-4.00005-X. Downstream Conversion, (2016), https://doi.org/10.2172/1239893.
[120] R.V. Pearsall, R.L. Connelly, M.E. Fountain, C.S. Hearn, M.D. Werst, R.E. Hebner, [145] A.B. Aragón, R.B. Padilla, J.A.F.R. de Ursinos, Experimental study of the recovery
E.F. Kelley, Electrically dewatering microalgae, IEEE Trans. Dielectr. Electr. Insul. of algae cultured in effluents from the anaerobic biological treatment of urban
18 (2011) 1578–1583, https://doi.org/10.1109/TDEI.2011.6032827. wastewaters, Resour. Conserv. Recycl. 6 (1992) 293–302, https://doi.org/10.
[121] S.K. Wang, A.R. Stiles, C. Guo, C.Z. Liu, Harvesting microalgae by magnetic se- 1016/0921-3449(92)90053-5.
paration: a review, Algal Res. 9 (2015) 178–185, https://doi.org/10.1016/j.algal. [146] P. Le-Clech, V. Chen, T.A.G. Fane, Fouling in membrane bioreactors used in
2015.03.005. wastewater treatment, J. Memb. Sci. 284 (2006) 17–53, https://doi.org/10.1016/
[122] M. Cerff, M. Morweiser, R. Dillschneider, A. Michel, K. Menzel, C. Posten, j.memsci.2006.08.019.
Harvesting fresh water and marine algae by magnetic separation: screening of [147] B.L. Marrone, R.E. Lacey, D.B. Anderson, J. Bonner, J. Coons, T. Dale,
separation parameters and high gradient magnetic filtration, Bioresour. Technol. C.M. Downes, S. Fernando, C. Fuller, B. Goodall, J.E. Holladay, K. Kadam, D. Kalb,
118 (2012) 289–295, https://doi.org/10.1016/j.biortech.2012.05.020. W. Liu, J.B. Mott, Z. Nikolov, K.L. Ogden, R.T. Sayre, B.G. Trewyn, J.A. Olivares,
[123] G. Prochazkova, I. Safarik, T. Branyik, Harvesting microalgae with microwave Review of the harvesting and extraction program within the National Alliance for
synthesized magnetic microparticles, Bioresour. Technol. 130 (2013) 472–477, Advanced Biofuels and Bioproducts, Algal Res. (2017), https://doi.org/10.1016/j.
https://doi.org/10.1016/j.biortech.2012.12.060. algal.2017.07.015.
[124] Y.-R. Hu, F. Wang, S.-K. Wang, C.-Z. Liu, C. Guo, Efficient harvesting of marine [148] J.E. Coons, D.M. Kalb, T. Dale, B.L. Marrone, Getting to low-cost algal biofuels: a
microalgae Nannochloropsis maritima using magnetic nanoparticles, Bioresour. monograph on conventional and cutting-edge harvesting and extraction technol-
Technol. 138 (2013) 387–390, https://doi.org/10.1016/j.biortech.2013.04.016. ogies, Algal Res. 6 (2014) 250–270, https://doi.org/10.1016/j.algal.2014.08.005.
[125] L. Xu, C. Guo, F. Wang, S. Zheng, C.-Z. Liu, A simple and rapid harvesting method [149] S.L. Pahl, A.K. Lee, T. Kalaitzidis, P.J. Ashman, S. Sathe, D.M. Lewis,
for microalgae by in situ magnetic separation, Bioresour. Technol. 102 (2011) M.A. Borowitzka, N.R. Moheimani (Eds.), Harvesting, Thickening and Dewatering
10047–10051. Microalgae Biomass BT - Algae for Biofuels and Energy, Springer, Netherlands,
17
M. Roy and K. Mohanty Algal Research 44 (2019) 101683
Dordrecht, 2013, pp. 165–185, , https://doi.org/10.1007/978-94-007-5479-9_10. [176] V.M. Rwehumbiza, R. Harrison, L. Thomsen, Alum-induced flocculation of pre-
[150] G. Singh, S.K. Patidar, Microalgae harvesting techniques: a review, J. Environ. concentrated Nannochloropsis salina: residual aluminium in the biomass, FAMEs
Manage. 217 (2018) 499–508, https://doi.org/10.1016/j.jenvman.2018.04.010. and its effects on microalgae growth upon media recycling, Chem. Eng. J. 200–202
[151] T. Mathimani, N. Mallick, A comprehensive review on harvesting of microalgae for (2012) 168–175, https://doi.org/10.1016/j.cej.2012.06.008.
biodiesel – key challenges and future directions, Renew. Sustain. Energy Rev. 91 [177] S.K. Gupta, N.M. Kumar, A. Guldhe, F.A. Ansari, I. Rawat, M. Nasr, F. Bux,
(2018) 1103–1120, https://doi.org/10.1016/j.rser.2018.04.083. Wastewater to biofuels: comprehensive evaluation ofvarious flocculants on bio-
[152] I. Rawat, R. Ranjith Kumar, T. Mutanda, F. Bux, Biodiesel from microalgae: a chemical composition and yield of microalgae, Ecol. Eng. 117 (2018) 62–68,
critical evaluation from laboratory to large scale production, Appl. Energy 103 https://doi.org/10.1016/j.ecoleng.2018.04.005.
(2013), https://doi.org/10.1016/j.apenergy.2012.10.004. [178] C.O. Letelier-Gordo, S.L. Holdt, D. De Francisci, D.B. Karakashev, I. Angelidaki,
[153] A.K. Lee, D.M. Lewis, P.J. Ashman, Microbial flocculation, a potentially low-cost Effective harvesting of the microalgae Chlorella protothecoides via bioflocculation
harvesting technique for marine microalgae for the production of biodiesel, J. with cationic starch, Bioresour. Technol. 167 (2014) 214–218, https://doi.org/10.
Appl. Phycol. 21 (2009) 559–567, https://doi.org/10.1007/s10811-008-9391-8. 1016/j.biortech.2014.06.014.
[154] M.Y.A. Mollah, P. Morkovsky, J.A.G. Gomes, M. Kesmez, J. Parga, D.L. Cocke, [179] M.S. Farid, A. Shariati, A. Badakhshan, B. Anvaripour, Using nano-chitosan for
Fundamentals, present and future perspectives of electrocoagulation, J. Hazard. harvesting microalga Nannochloropsis sp, Bioresour. Technol. 131 (2013)
Mater. 114 (2004), https://doi.org/10.1016/j.jhazmat.2004.08.009. 555–559, https://doi.org/10.1016/j.biortech.2013.01.058.
[155] X. Zou, Y. Li, K. Xu, H. Wen, Z. Shen, X. Ren, Microalgae harvesting by buoy-bead [180] L. Van Haver, S. Nayar, Polyelectrolyte flocculants in harvesting microalgal bio-
flotation process using Bioflocculant as alternative to chemical Flocculant, Algal mass for food and feed applications, Algal Res. 24 (2017) 167–180, https://doi.
Res. 32 (2018) 233–240, https://doi.org/10.1016/j.algal.2018.04.010. org/10.1016/j.algal.2017.03.022.
[156] G. Kandasamy, S.R.M. Shaleh, Flotation removal of the microalga Nannochloropsis [181] F. Bleeke, M. Milas, D. Winckelmann, G. Klöck, Optimization of freshwater mi-
sp. Using Moringa protein–oil emulsion: a novel green approach, Bioresour. croalgal biomass harvest using polymeric flocculants, Int. Aquat. Res. 7 (2015)
Technol. 247 (2018) 327–331, https://doi.org/10.1016/j.biortech.2017.08.187. 235–244, https://doi.org/10.1007/s40071-015-0108-8.
[157] Z. Shen, Y. Li, H. Wen, X. Ren, J. Liu, L. Yang, Investigation on the role of sur- [182] C.M.L.L. Teixeira, F.V. Kirsten, P.C.N. Teixeira, Evaluation of Moringa oleifera
factants in bubble-algae interaction in flotation harvesting of Chlorella vulgaris, seed flour as a flocculating agent for potential biodiesel producer microalgae, J.
Sci. Rep. 8 (2018) 3303, https://doi.org/10.1038/s41598-018-21629-x. Appl. Phycol. 24 (2012) 557–563, https://doi.org/10.1007/s10811-011-9773-1.
[158] W. Zhou, L. Gao, W. Cheng, L. Chen, J. Wang, H. Wang, W. Zhang, T. Liu, Electro- [183] P. Lopez-Exposito, C. Campano, T.G.M. van de Ven, C. Negro, A. Blanco,
flotation of Chlorella sp. assisted with flocculation by chitosan, Algal Res. 18 Microalgae harvesting with the novel flocculant hairy cationic nanocrystalline
(2016) 7–14, https://doi.org/10.1016/j.algal.2016.05.029. cellulose, Colloids Surf. B Biointerfaces 178 (2019) 329–336, https://doi.org/10.
[159] T. Coward, J.G.M. Lee, G.S. Caldwell, Harvesting microalgae by CTAB-aided foam 1016/j.colsurfb.2019.03.018.
flotation increases lipid recovery and improves fatty acid methyl ester character- [184] W. Zhou, M. Min, B. Hu, X. Ma, Y. Liu, Q. Wang, J. Shi, P. Chen, R. Ruan,
istics, Biomass Bioenergy 67 (2014) 354–362. Filamentous fungi assisted bio-flocculation: a novel alternative technique for
[160] X. Zou, K. Xu, H. Wen, Y. Xue, S. Zhao, W. Xie, Y. Li, A novel method to recover harvesting heterotrophic and autotrophic microalgal cells, Sep. Purif. Technol.
microalgae by compound buoyant-bead flotation, Sep. Purif. Technol. 211 (2019) 107 (2013) 158–165.
658–666, https://doi.org/10.1016/j.seppur.2018.10.047. [185] T.D.P. Nguyen, T.V.A. Le, P.L. Show, T.T. Nguyen, M.H. Tran, T.N.T. Tran,
[161] M.A.S. Alkarawi, G.S. Caldwell, J.G.M. Lee, Continuous harvesting of microalgae S.Y. Lee, Bioflocculation formation of microalgae-bacteria in enhancing micro-
biomass using foam flotation, Algal Res. 36 (2018) 125–138, https://doi.org/10. algae harvesting and nutrient removal from wastewater effluent, Bioresour.
1016/j.algal.2018.10.018. Technol. 272 (2019) 34–39, https://doi.org/10.1016/j.biortech.2018.09.146.
[162] S. Garg, L. Wang, P.M. Schenk, Flotation separation of marine microalgae from [186] T. Ndikubwimana, X. Zeng, T. Murwanashyaka, E. Manirafasha, N. He, W. Shao,
aqueous medium, Sep. Purif. Technol. 156 (2015) 636–641, https://doi.org/10. Y. Lu, Harvesting of freshwater microalgae with microbial bioflocculant: a pilot-
1016/j.seppur.2015.10.059. scale study, Biotechnol. Biofuels 9 (2016) 47, https://doi.org/10.1186/s13068-
[163] K. Xu, Y. Li, X. Zou, H. Wen, Z. Shen, X. Ren, Investigating microalgae cell-mi- 016-0458-5.
crosphere interactions during microalgae harvesting by ballasted dissolved air [187] E. Díaz-Santos, M. Vila, M. de la Vega, R. León, J. Vigara, Study of bioflocculation
flotation through XDLVO theory, Biochem. Eng. J. 137 (2018) 294–304, https:// induced by Saccharomyces bayanus var. uvarum and flocculating protein factors
doi.org/10.1016/j.bej.2018.06.013. in microalgae, Algal Res. 8 (2015) 23–29.
[164] F. Wicaksana, A.G. Fane, P. Pongpairoj, R. Field, Microfiltration of algae (Chlorella [188] M. Agbakpe, S. Ge, W. Zhang, X. Zhang, P. Kobylarz, Algae harvesting for biofuel
sorokiniana): critical flux, fouling and transmission, J. Memb. Sci. 387–388 (2012) production: influences of UV irradiation and polyethylenimine (PEI) coating on
83–92, https://doi.org/10.1016/j.memsci.2011.10.013. bacterial biocoagulation, Bioresour. Technol. 166 (2014) 266–272, https://doi.
[165] S. Babel, S. Takizawa, H. Ozaki, Factors affecting seasonal variation of membrane org/10.1016/j.biortech.2014.05.060.
filtration resistance caused by Chlorella algae, Water Res. 36 (2002) 1193–1202, [189] J. Chen, L. Leng, C. Ye, Q. Lu, M. Addy, J. Wang, J. Liu, P. Chen, R. Ruan, W. Zhou,
https://doi.org/10.1016/S0043-1354(01)00333-5. A comparative study between fungal pellet- and spore-assisted microalgae har-
[166] W. Zhang, W. Zhang, X. Zhang, P. Amendola, Q. Hu, Y. Chen, Characterization of vesting methods for algae bioflocculation, Bioresour. Technol. 259 (2018)
dissolved organic matters responsible for ultrafiltration membrane fouling in algal 181–190, https://doi.org/10.1016/j.biortech.2018.03.040.
harvesting, Algal Res. 2 (2013) 223–229, https://doi.org/10.1016/j.algal.2013. [190] S. Luo, X. Wu, H. Jiang, M. Yu, Y. Liu, A. Min, W. Li, R. Ruan, Edible fungi-assisted
05.002. harvesting system for efficient microalgae bio-flocculation, Bioresour. Technol.
[167] F. Zhao, H. Chu, Y. Su, X. Tan, Y. Zhang, L. Yang, X. Zhou, Microalgae harvesting 282 (2019) 325–330, https://doi.org/10.1016/j.biortech.2019.03.033.
by an axial vibration membrane: the mechanism of mitigating membrane fouling, [191] F. Bleeke, G. Quante, D. Winckelmann, G. Klöck, Effect of voltage and electrode
J. Memb. Sci. 508 (2016) 127–135, https://doi.org/10.1016/j.memsci.2016.02. material on electroflocculation of Scenedesmus acuminatus, Bioresour. Bioprocess.
007. 2 (2015) 36, https://doi.org/10.1186/s40643-015-0064-6.
[168] A.L. Ahmad, N.H.M. Yasin, C.J.C. Derek, J.K. Lim, Harvesting of microalgal bio- [192] N. Fayad, T. Yehya, F. Audonnet, C. Vial, Harvesting of microalgae Chlorella
mass using MF membrane: kinetic model, CDE model and extended DLVO theory, vulgaris using electro-coagulation-flocculation in the batch mode, Algal Res. 25
J. Memb. Sci. 446 (2013) 341–349, https://doi.org/10.1016/j.memsci.2013.07. (2017) 1–11, https://doi.org/10.1016/j.algal.2017.03.015.
012. [193] A. Rahmani, D. Zerrouki, L. Djafer, A. Ayral, Hydrogen recovery from the pho-
[169] X. Chen, C. Huang, T. Liu, Harvesting of microalgae Scenedesmus sp. using tovoltaic electroflocculation-flotation process for harvesting Chlorella pyrenoidosa
polyvinylidene fluoride microfiltration membrane, Desalin. Water Treat. 45 microalgae, Int. J. Hydrogen Energy 42 (2017) 19591–19596, https://doi.org/10.
(2012) 177–181, https://doi.org/10.1080/19443994.2012.692034. 1016/j.ijhydene.2017.06.123.
[170] A. Jana, S. Ghosh, S. Majumdar, Energy efficient harvesting of Arthrospira sp. [194] E. Valero, X. Álvarez, Á. Cancela, Á. Sánchez, Harvesting green algae from eu-
using ceramic membranes: analyzing the effect of membrane pore size and in- trophic reservoir by electroflocculation and post-use for biodiesel production,
corporation of flocculant as fouling control strategy, J. Chem. Technol. Biotechnol. Bioresour. Technol. 187 (2015) 255–262, https://doi.org/10.1016/j.biortech.
93 (2018) 1085–1096, https://doi.org/10.1002/jctb.5466. 2015.03.138.
[171] D. Kim, M. Kwak, K. Kim, Y.K. Chang, Turbulent jet-assisted microfiltration for [195] C.T. Matos, M. Santos, B.P. Nobre, L. Gouveia, Nannochloropsis sp. biomass re-
energy efficient harvesting of microalgae, J. Memb. Sci. 575 (2019) 170–178, covery by Electro-Coagulation for biodiesel and pigment production, Bioresour.
https://doi.org/10.1016/j.memsci.2018.12.069. Technol. 134 (2013) 219–226, https://doi.org/10.1016/j.biortech.2013.02.034.
[172] Y. Zhang, X. Li, R. Xu, C. Ma, X. Wang, Q. Fu, Algal fouling control in a hollow [196] R. Misra, A. Guldhe, P. Singh, I. Rawat, T.A. Stenström, F. Bux, Evaluation of
fiber module during ultrafiltration by angular vibrations, J. Memb. Sci. 569 (2019) operating conditions for sustainable harvesting of microalgal biomass applying
200–208, https://doi.org/10.1016/j.memsci.2018.10.029. electrochemical method using non sacrificial electrodes, Bioresour. Technol. 176
[173] I. de Godos, H.O. Guzman, R. Soto, P.A. García-Encina, E. Becares, R. Muñoz, (2015) 1–7, https://doi.org/10.1016/j.biortech.2014.11.014.
V.A. Vargas, Coagulation/flocculation-based removal of algal–bacterial biomass [197] F. Baierle, D.K. John, M.P. Souza, T.R. Bjerk, M.S.A. Moraes, M. Hoeltz,
from piggery wastewater treatment, Bioresour. Technol. 102 (2011) 923–927, A.L.B. Rohlfes, M.E. Camargo, V.A. Corbellini, R.C.S. Schneider, Biomass from
https://doi.org/10.1016/j.biortech.2010.09.036. microalgae separation by electroflotation with iron and aluminum spiral elec-
[174] L. Chen, C. Wang, W. Wang, J. Wei, Optimal conditions of different flocculation trodes, Chem. Eng. J. 267 (2015) 274–281, https://doi.org/10.1016/j.cej.2015.
methods for harvesting Scenedesmus sp. Cultivated in an open-pond system, 01.031.
Bioresour. Technol. 133 (2013) 9–15, https://doi.org/10.1016/j.biortech.2013. [198] A. Landels, T.A. Beacham, C.T. Evans, G. Carnovale, S. Raikova, I.S. Cole,
01.071. P. Goddard, C. Chuck, M.J. Allen, Improving electrocoagulation floatation for
[175] S. Sirin, R. Trobajo, C. Ibanez, J. Salvadó, Harvesting the microalgae harvesting microalgae, Algal Res. 39 (2019) 101446, , https://doi.org/10.1016/j.
Phaeodactylum tricornutum with polyaluminum chloride, aluminium sulphate, algal.2019.101446.
chitosan and alkalinity-induced flocculation, J. Appl. Phycol. 24 (2012) [199] E. Boli, M. Savvidou, D. Logothetis, V. Louli, G. Pappa, E. Voutsas, F. Kolisis,
1067–1080, https://doi.org/10.1007/s10811-011-9736-6. K. Magoulas, Magnetic harvesting of marine algae Nannochloropsis oceanica, Sep.
18
M. Roy and K. Mohanty Algal Research 44 (2019) 101683
Sci. Technol. 0 (2017) 1–8, https://doi.org/10.1080/01496395.2017.1296463. processes for microalgae biomass production: a perspective from patent literature,
[200] G. Prochazkova, N. Podolova, I. Safarik, V. Zachleder, T. Branyik, Physicochemical Algal Res. 31 (2018) 469–477, https://doi.org/10.1016/j.algal.2018.01.016.
approach to freshwater microalgae harvesting with magnetic particles, Colloids [206] B. Barrut, J.-P. Blancheton, M. Callier, J.-Y. Champagne, A. Grasmick, Foam
Surf. B Biointerfaces 112 (2013) 213–218, https://doi.org/10.1016/j.colsurfb. fractionation efficiency of a vacuum airlift—application to particulate matter re-
2013.07.053. moval in recirculating systems, Aquac. Eng. 54 (2013) 16–21, https://doi.org/10.
[201] J.Y. Seo, K. Lee, R. Praveenkumar, B. Kim, S.Y. Lee, Y.-K. Oh, S. Bin Park, Tri- 1016/j.aquaeng.2012.10.003.
functionality of Fe3O4-embedded carbon microparticles in microalgae harvesting, [207] M.R. Bilad, G. Mezohegyi, P. Declerck, I.F.J. Vankelecom, Novel magnetically
Chem. Eng. J. 280 (2015) 206–214, https://doi.org/10.1016/j.cej.2015.05.122. induced membrane vibration (MMV) for fouling control in membrane bioreactors,
[202] K. Lee, J.-G. Na, J.Y. Seo, T.S. Shim, B. Kim, R. Praveenkumar, J.-Y. Park, Y.-K. Oh, Water Res. 46 (2012) 63–72, https://doi.org/10.1016/j.watres.2011.10.026.
S.G. Jeon, Magnetic-nanoflocculant-assisted water–nonpolar solvent interface [208] N.K. Sahoo, S.K. Gupta, I. Rawat, F.A. Ansari, P. Singh, S.N. Naik, F. Bux,
sieve for microalgae harvesting, ACS appl. Mater. Interfaces 7 (2015) Sustainable dewatering and drying of self-flocculating microalgae and study of
18336–18343, https://doi.org/10.1021/acsami.5b04098. cake properties, J. Clean. Prod. 159 (2017) 248–256, https://doi.org/10.1016/j.
[203] J.Y. Seo, R. Praveenkumar, B. Kim, J.-C. Seo, J.-Y. Park, J.-G. Na, S.G. Jeon, S. Bin jclepro.2017.05.015.
Park, K. Lee, Y.-K. Oh, Downstream integration of microalgae harvesting and cell [209] R. Misra, A. Guldhe, P. Singh, I. Rawat, F. Bux, Electrochemical harvesting process
disruption by means of cationic surfactant-decorated Fe3O4 nanoparticles, Green for microalgae by using nonsacrificial carbon electrode: a sustainable approach for
Chem. 18 (2016) 3981–3989, https://doi.org/10.1039/C6GC00904B. biodiesel production, Chem. Eng. J. 255 (2014) 327–333, https://doi.org/10.
[204] K. Lee, S.Y. Lee, R. Praveenkumar, B. Kim, J.Y. Seo, S.G. Jeon, J.-G. Na, J.-Y. Park, 1016/j.cej.2014.06.010.
D.-M. Kim, Y.-K. Oh, Repeated use of stable magnetic flocculant for efficient [210] J. Kim, B.-G. Ryu, B.-K. Kim, J.-I. Han, J.-W. Yang, Continuous microalgae re-
harvest of oleaginous Chlorella sp, Bioresour. Technol. 167 (2014) 284–290, covery using electrolysis with polarity exchange, Bioresour. Technol. 111 (2012)
https://doi.org/10.1016/j.biortech.2014.06.055. 268–275, https://doi.org/10.1016/j.biortech.2012.01.104.
[205] N. Deconinck, K. Muylaert, W. Ivens, D. Vandamme, Innovative harvesting
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