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Algal Research 44 (2019) 101683

Contents lists available at ScienceDirect

Algal Research
journal homepage: www.elsevier.com/locate/algal

Review article

A comprehensive review on microalgal harvesting strategies: Current status T


and future prospects
Madonna Roya, Kaustubha Mohantya,b,*
a
Centre for Energy, Indian Institute of Technology Guwahati, Guwahati 781 039, India
b
Department of Chemical Engineering, Indian Institute of Technology Guwahati, Guwahati 781039, India

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

density of the freshwater green microalgae (Chlorococcum) ranges

[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.

Stokes’ Law (Eq.1), the hypothetical settlement velocity of one single


spherical shaped microalgal cell such as Chlorella was determined to be
0.1 m day-1 [32]. The settling velocity of diatoms, green microalgae and
cyanobacteria were found to be 0.2 m day-1, 0.1 m day-1 and 0 to
application
Large scale

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

tend to have a diverse range of shapes as a result of evolutionary de-


velopment. This morphological development of microalgae prevents
medium

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

Surfactant may be toxic

Metal contamination

Metal contamination
Metal contamination

[38]. While studying the sinking rate of 30 microalgae species collected


from wastewater, it was found that most of them were reluctant to
cause toxicity

settle, particularly the needle-shaped microalgae [39]. Studies show the


No toxicity

No toxicity

No toxicity

possibility of harvesting colonial algae such as Micractinium and Sce-


Toxicity

nedesmus (with a cluster diameter of approximately 60 μm) via sedi-


mentation. However, sedimentation is not possible for smaller micro-
algae such as Chlorella and motile algae such as Euglena and
Operational cost

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

is comparatively low. Generally, a lamella type settling tank consumes


Process time

0.1 kWh m−3 for obtaining 0.1%–1.5% dry microalgal biomass [45]. As
Medium

the process is non-turbulent or high-pressure-driven, it preserves the


Short

Short
Short

Short

Short
Short
Short
Long

structural integrity of the microalgae [46] and requires low energy


[47]. During harvesting, sedimentation is generally used as a pre-con-
Cell damage

centration step for settling colonial and large-sized microalgae.


Harvesting of biomass by sedimentation is a cost-effective, effortless
and simple technique, as the process does not require any energy or
Yes

Yes
No

No
No

No
No
No

No

addition of chemicals. Nevertheless, this process is time-consuming,


Comparison of various harvesting techniques.

unreliable, and there is a probability of biomass deterioration, which


hinders its commercial application.
efficiency
Recovery

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

ciency of harvesting depends on the microalgae cell size and density


Harvesting techniques

difference between the microalgae biomass and the medium. The set-
Electroflocculation

tling rate is boosted by the high rotational speed of the centrifuge. In


Autoflocculation
Bioflocculation

harvesting
Centrifugation
Sedimentation

reality, centrifugation is an extension of gravity sedimentation, and the


Flocculation

cell settling velocity is given by:


Filtration
Flotation
Table 1

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]).

3.1.4. Filtration filtration is classified as microfiltration, ultrafiltration, nanofiltration


The recovery of microalgal biomass by filtration involves a semi- and reverse/forward osmosis [63]. Darcy’s equation defines the per-
permeable membrane that acts as a filter to separate solid from liquid. formance of membrane filtration processes [64].
This semi-permeable filter is comprised of pores smaller than the cells
being retained, allowing selective passage of substances smaller in size ΔP − ΔΠ
J=
than the pores of the filter. Membrane filtration processes mainly in- (Rm + R c ) μ (4)
volve two flow configurations: dead-end and tangential flow. In case of
dead-end membrane filtration, the flow is perpendicular to the mem- where J denotes the membrane flux (m3 (m2·s)−1), ΔP denotes the
brane surface. Dead-end filtration is generally a batch process, where transmembrane pressure (Pa), ΔΠ denotes the osmotic pressure (Pa), Rm
cartridge filtration, vacuum drum filters, and horizontal filter press are denotes the intrinsic membrane resistance (m− 1), Rc denotes the cake
the three common technologies that work in dead-end mode. In tan- resistance owing to fouling (m− 1) and μ denotes the viscosity of the
gential membrane filtration, the flow is tangential to the membrane microalgae suspension (Pa·s).
surface. Tangential flow filtration (TFF) consists of synthetic semi- Harvesting of microalgae through membrane filtration is usually
permeable membranes with pore sizes ranging from a few Angstroms to carried out within the ultrafiltration-microfiltration range [65]. For-
a few Microns. Based on the pore size of the membrane, the membrane ward osmosis membrane process is the optimum membrane filtration
technique for the harvesting of microalgal biomass from dilute media as

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

it also helps to reduce power consumption [66]. Membrane filtration

[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

Volumetric concentration factor


steady-state permeance. On the other hand, some researchers con-
cluded that applying an ultrafiltration membrane is pointless, as lower
initial fluxes and higher operating pressures overshadow better per-
formance [68]. Drawbacks of using membrane filtration include
membrane pore blocking, cake formation and adsorption of gel-foulants
such as EOM. Fouling can be reduced by back-flushing [69], membrane
surface modification, addition of coagulants, dynamic filtration and

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-

19 × 106 cells ml−1


Algal concentration
plicable for shear-sensitive species. Moreover, the process allows the

0.9–1.2 cells L−1


reusability of the medium. The filtration process is non-toxic and thus,

−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

3.2. Chemical methods


∼0.01 μm

∼0.02 μm
0.45 μm

3.2.1. Inorganic flocculation


∼1 μm
50 kDa
0.2 μm

0.1 μm
1.2 μm
0.2 μm

0.2 μm

Natural settling of microalgae is not possible always because most of


the algal cells are small in size with a negatively charged cell surface.
So, to enhance the settling rates, pre-flocculation is generally carried
out which confirm settling rates of ≥ 0.6 cm/s [43]. The negatively
Polyvinylidene di-fluoride

polyvinylidene di-fluoride

polyvinylidene di-fluoride

charged cell surface of microalgae leads to ionization of functional


polyvinylidene fluoride
Anopore inorganic disc

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

organic matter [72]. Hence, auto-aggregation is not viable because of


the repulsion of negatively charged cells. Aggregation of microalgal
cells require the negatively charged cell surface to be neutralized by the
Ceramic

addition of flocculants [72]. Charge dispersion is the concept followed


by flocculation method [73]. This harvesting method specifically causes
ionic interaction between cells and flocculants and salts existing in the
growth medium [74].
Axial vibration membrane

In all the approaches of flocculation, small algal cells suspended in


the growth medium are combined to form large aggregates followed by
Membrane filtration

the accumulation of aggregates into bigger flocs [75]. Flocculation is


Filtration method

Microfiltration

Microfiltration
Microfiltration

Microfiltration
Microfiltration

usually used in combination with other harvesting techniques [28]. The


Ultrafiltration

Ultrafiltration

Ultrafiltration

settling rate can be enhanced through flocculation as it results in the


aggregation of microalgal cells, thus increasing the size of the particles
[76]. Flocculation being able to settle huge quantities and a wide range
of microalgae becomes a superior technique to harvest algae [42]. Al-
though the flocculation process is expensive, still it has been recognized
as the most reliable method [77]. Studies found that flocculation can be
Scenedesmus quadricauda

persuaded by chemicals, both inorganic and organic, or by micro-


Chlorella pyrenoidosa
Chlorella sorokiniana

organisms, or by natural flocculants, but the retrieval and recycling of


Chlorella vulgaris
Scenedesmus sp.

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

friendly; (c) be inexpensive and non-toxic so that it can be applied in


Table 3

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

Requires high coagulant dose, pH sensitive, residual iron in microalgal biomass


solution of cationic salts in the growth medium releases its respective
cations, which neutralizes or reduces the electrostatic force of repulsion
between the algal cells, enabling the cells to form large flocs [73].

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

divalent cationic salts [12].


Chlorella cells were more efficiently flocculated by the addition of
aluminum salts in comparison to ferric salts [78]. With respect to op-
timal flocculant dose, pH and quality of the resultant medium, alum
High coagulant dose results in cell damage

High coagulant dose results in cell damage


pH dependent, damage of microalgal cells

was found to be superior to ferric salt. The high solubility of chloride at


pH depended, and risk of contamination

a wide concentration range enables the salt to attain maximum floc-


culation efficiency as compared to sulfate salts [78]. Studies found that
lower electronegativity of CaSO4, CaCl2, MgSO4, MgCl2, (NH4)2SO4,
Requires high coagulant dose

Requires high coagulant dose

Requires high coagulant dose

and NH4Cl salts resulted in lower harvesting efficiency [78].


Harvesting of biomass by inorganic flocculation is simple, fast,
highly efficient and economical as no energy is required. However,
inorganic flocculants tend to have adverse effects on algal cells. It may
also change the colour and modify the chemical composition of the
algal growth medium, making it unsuitable for reuse [77]. Although
Features

inorganic flocculants such as iron and aluminum salts are relatively


inexpensive compared to most synthetic organic flocculants, the higher
concentration required to accomplish high flocculation efficiency ulti-
R (%)

82.60

66.60
≥90

≥85

≥95

mately increases the cost of harvesting. This also generates a huge


98

98

90

95
80
90
99
66

98

quantity of sludge [48]. Inorganic flocculants work on specific micro-


algal species. Flocculation efficiency of inorganic flocculants is low in
Process time (min)

marine water, as it tends to coil in the high ionic environment; hence,


inorganic flocculants are not suitable for harvesting marine microalgae
[22].
Comparison of several inorganic flocculants based on their efficacy of harvesting various microalgal strains.

180

240
10
10

10

10
30
10

10
15
10

10

3.2.2. Organic flocculants


Organic flocculants are natural or synthetic polymers that are either
Flocculant dose

branched or linear and carrying cationic, anionic or non-ionic charge


150 mg L−1

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

[79]. However, as the microalgal cell surface is negatively charged, the


1 g L−1
30 ppm

30 ppm

role of anionic or non-ionic flocculants becomes insignificant [42].


Unlike inorganic flocculants, organic polymer flocculants with varying
physicochemical properties are highly efficient even in low doses of a
3.11 ± 0.09 × 106 cells mL−1

3.11 ± 0.09 × 106 cells mL−1

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

tion. Coagulation is defined as a process by which a stabilized particle is


destabilized by addition of a chemical compound, i.e., coagulant. On
10-20 g L−1

the contrary, flocculation is the coalescence of separate suspended


0.54 g L−1

microalgal cells into larger loosely attached conglomerates [80]. Ca-


tionic polymers neutralize the negative charge carried on the micro-




algal cell surface and simultaneously binds to the surface of two or


more algal cells, thus, forming a bridge among the destabilized particles
Aluminum nitrate sulfate

[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

cause potent neurotoxic effects [82]. However, the overall efficacy of


Alum
FeCl3

FeCl3

FeCl3

FeCl3
NH3

PAC

Polyaluminium chloride (PAC).

synthetic versus natural polymers depends on several factors such as


pH, salinity, biomass concentration, and algal organic matter (AOM)
[83]. In general, non-toxic and biodegradable natural polymeric floc-
Phaeodactylum tricornutum

Phaeodactylum tricornutum

culants such as starch, cellulose, and chitosan have received more in-
Chlorella minutissima

terest as compared to synthetic flocculants [84]. It has been reported


Chlorococcum sp.
Scenedesmus sp.

Scenedesmus sp.

that 30 ppm of cationic locust bean gum biopolymer could successfully


C. sorokiniana

C. sorokiniana

C. sorokiniana
Chlorella sp.

Chlorella sp.
Microalgae

harvest 97.42% of Scenedesmus sp. [85]. One of the major drawbacks of


S. obliquus

S. obliquus
N. salina

polymeric flocculants is that they fail to flocculate marine algae. The


Table 4

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

The high ionic strength of the marine environment attributes to the

[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].

Reusability of the medium; pH dependent, more feasible than


No contamination problem, pH dependent, cost prohibitive
Chitosan is a natural polymeric flocculant with enhanced cationicity

pH independent; harvested microalgal cells remains intact

Requires high coagulant dose, low toxicity, less expensive


and is efficient in flocculating both fresh and marine microalgae at low

Not effective for harvesting marine microalgae, non-


pH without contaminating the microalgal biomass [23]. However,
chitosan requires high dose (20–150 mg L−1) as compared to other
synthetic flocculants and is too expensive to be used for industrial-scale
[31]. Chitosan is replaced by cationic starch, which is not too expensive

Efficient, cost effective, pH dependent

simple, efficient, inexpensive method

simple, efficient, inexpensive method

Efficient, economical, pH dependent


and pH-dependent; however, it works at higher concentration [87].

Non-biodegradable, carcinogenic
Cellulose modification by introducing the desired functionality is a
novel approach for increasing the flocculant efficiency. Highly cationic

Poor harvesting efficiency


cellulose nanocrystals (CNCs) synthesized by grafting cationic pyr-
idinium groups on CNCs isolated from cotton wool were relatively in-

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

Organic flocculants can harvest huge amount of biomass easily and

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

1 × 107 cells ml−1

1 × 107 cells ml−1


1 × 107 cells ml−1

1 × 107 cells ml−1


0.56-0.77 g L−1

3.3. Biological methods

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

study found that high pH, usually above pH 9 induces autoflocculation


Polyelectrolyte
Nanocellulose
Polymer type

Potato starch

[93]. In case of a high pH-induced autoflocculation, the cell wall in-


Polystyrene

teracts with divalent cations [94]. Calcium and phosphate ions get
supersaturated with the increase of pH, causing the neutralization of
salt



the microalgal cells that are negatively charged by the positively


charged calcium phosphate precipitate [12]. However, a prerequisite
Moringa oleifera seed flour

amount of phosphate (0.0031–0.0062 g L−1) and calcium (0.06–0.1 g


Hairy cationic nanocrystalline cellulose (CNCC).
POLY SEPAR® KW100
POLY SEPAR® CFL25

L−1) is required to achieve autoflocculation at 8.5–9 pH [95]. Some


Cationic polyamine

Magnafloc LT225

researchers have reported achieving 80% flocculation efficiency by


Cationic starch

Nano-chitosan

Emfloc KC750

replacing calcium and phosphate by the addition of lime [96]. A fast


Zetag 8819
Flocculants

Chitosan
polymer

and cost-effective way of harvesting can be achieved by increasing the


CNCC
EM22
A-21

pH of the medium by stopping the CO2 supply.


Knuckey et al. [97] obtained 97 ± 2% settling efficiency at pH 10
for Scenedesmus. He observed that at pH 10, the flocs lead to the for-
Chlamydomonas reinhardtii
Phaeodactylum tricornutum

Scenedesmus acuminatus

mation of a robust structure due to which high settling efficiency was


Chlorella sorokiniana
Nannochloropsis sp.

obtained.
Chlorella vulgaris
C. protothecoides
Scenedesmus sp.

Muriellopsis sp.

Autoflocculation is a simple, inexpensive and chemical-free non-


Chlorella sp.
Chlorella sp.

Chlorella sp.

toxic process. Nonetheless, it is not fit for industrial-scale harvesting, as


Chlorophyta
Microalgae

it is time consuming, unreliable and suits only a few microalgae species


Table 5

[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-

Harvested biomass can be used for feed or food


vesting process, algal cells aggregate with the microorganisms (algae,

Affects microalgal cell integrity to some extent

Biochemical composition of biomass remains


bacteria, fungi) to form large flocs and finally settle down by gravi-

Depends on extracted protein concentration


bio-flocculant can be recycled and reused
metric force without the addition of any chemical flocculants. Floccu-
lant can also be extracted from an organism to flocculate microalgae;
such a process is known as biochemical flocculation. In biochemical

Chance of fungal contamination


flocculation, microalgae flocculate with the help of the extracellular

Requires high glucose input


Reusability of the medium
polymers and proteins that are extracted from an organism [101]. The
efficiency of bioflocculation depends on the quantity of extracellular

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-

240.0 × 106 CFU mL−1


1.2 × 104 spores mL−1

1.1 × 104 spores mL−1


glutamic acid produced by Bacillus licheniformis CGMCC 2876 was
successful in harvesting Desmodesmus sp. F51 with a recovery efficiency

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

Further, a symbiotic relationship was observed between microalgae

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-

non-coagulative methods [107]. In coagulative process, the spores ag-


gregate with microalgae to form pellets. Aspergillus sp., Basidiomycete
sp. and Phanerochaete sp. flocculates microalgae through a coagulative
method by forming dense spherical aggregates [107]. Whereas, in non-
Flocculant type
Recovery of microalgal biomass by bio-flocculation and sedimentation.

Bioflocculant

Bioflocculant

coagulative process, the hyphae germinated from the spores interlinks


flocculants

to form aggregates. The fungal strains such as Rhizopus sp., Mucor sp.
γ-PGA

γ-PGA

and Penicillium sp. flocculates microalgae through a non-coagulative


FPA
FSA

FSA
EPS

PEI

process [107]. These non-coagulative pellet strains have lower hydro-


phobicity, shorter germination period and higher growth rate as com-
pared to coagulative pellet strains. These properties of non-coagulative
Bacteria in seafood wastewater

Tap water bacterial inoculum

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,

minate after 5 h of cultivation, whereas A. niger spores germinate after


Aspergillus oryzae

Escherichia coli
Bacillus subtilis

8–10 h of cultivation [110–112]. Fungus mediated flocculation does not


Penicillium sp.
Bioflocculant

require any additional energy or chemicals to be added, thus, making


effluent

the harvesting process sustainable. Table 6 details various bio-


flocculants used for recovering microalgal biomass.
Bioflocculation is an energy-efficient, eco-friendly and chemical-
Nannochloropsis oceanica

Desmodesmus brasiliensis

free process that maintains cell integrity. Nonetheless, this harvesting


Pleurochrysis carterae

Chlorella zofingiensis

process is unreliable, as the process of flocculation is uncontrolled.


Chlorella vulgaris

Chlorella vulgaris
Chlorella vulgaris

Moreover, bioflocculation requires relatively high organic carbon


C. reinhardtii

Chlorella sp.
Chlorella sp.

source to cultivate autoflocculating microorganisms (such as algae,


Microalgae

bacteria, and fungi) for flocculating microalgae. High chances of mi-


Table 6

crobiological contamination stand as the major drawback of this har-


vesting technique.

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 quality was retained


Thus, achieving efficient harvesting with a high current density is im-

Pilot plant can be designed


Better than iron electrodes

Reusability of the medium

Electrolyte improved lipid


Lipid content not effected
practical without maintaining an equilibrium between current density

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

achieved when flotation was carried out post electroflocculation [118].


With the rise of process temperature, cell collision and their transpor-
tation rate tends to increase [116]. In a harvesting experiment con-
99 (pH 4)

83 (pH 9)
78.9 (pH

ducted by ECF technology, an increase in harvesting efficiency from


100 (pH
R (%)

95.83

> 97

46% to 98% was observed with the rise in temperature from 18 °C to


4–7)

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

[75]. Therefore, the reduction of electrolysis time helps to reduce the


process energy consumption.
(min)

Properties such as pH, initial cell concentration, and ionic strength


9.2
45

45

60

10

20

of the medium tend to affect the transport of algal cells [119]. The type
5
1

of metal ions formed in the electrolytic process depends on the pH of


Electrode material

the medium. In acidic conditions monomeric hydroxoaluminum ca-


inert titanium
Nonsacrificial
Magnesium

tions, aluminum hydroxide and cationic polymeric species are formed.


Aluminum

Aluminum
Aluminum
Aluminum

Aluminum

Aluminum

Electro-coagulation-flotation (ECF); Electro-flocculation (EF); Electro-Coagulation (EC); Dry weight (DW); Electrochemical harvesting (ECH).

These cationic species are easily absorbed by the negatively charged


iron

microalgal cells, thus, enhancing the settling process. On the other


hand, in a pH range of 8–14, monomeric hydroxoaluminum anions are
formed in the electrolytic solution, which offers resistance by de-
creasing the absorption capacity of microalgal cells [75]. Similarly, it
Cuurent/ Current

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

density of 2.10 × 109 cells L−1 required 75 min [116].


The high ionic strength of the marine microalgae enables them to be
Working volume

easily harvested, whereas freshwater microalgae require double energy


and settling time due to its low ionic strength [117]. As there is little
chance of flocculant contamination, the harvested biomass is safe for
1000

1000

1000

the use of animal feed or food [115]. However, electroflocculation


(mL)

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

1.84 × 107 cells mL−1

Electro-flocculation is a strain-independent and chemical-free pro-


Algal concentration

1 × 107 cells ml−1

cess. However, the high power density involved in this harvesting


2.2 ± 0.15 g L−1

process may impair cell integrity. There is also a high chance of cathode
106 cell ml−1

fouling. Thus, electro-flocculation, being a power induced process with


9
Recovery of microalgal biomass by electrical harvesting technique.

2.5 g DW

high electrophoretic equipment cost fails to be applicable for large-


scale.


Flocculation type

3.5. Magnetic particle assisted harvesting

In recent years, magnetophoretic separation of microalgae has


gained much attention due to its potential over traditional harvesting
ECH
ECF

ECF

ECF

ECF
EC
EF

EF
EF

EF

techniques. Magnetic particles assisted harvesting is based on simple


separation method in which micro or nano-sized magnetic particles are
Scenedesmus sp., Kirchneriella sp. and

adsorbed by the suspended microalgal cells [121]. The magnetic par-


ticle tagged cells are recovered based on their intrinsic paramagnetic
movement owing to the external magnetic force [122]. An ideal mag-
netic particle should be cost-effective, non-toxic, stable, reusable and
Scenedesmus acuminatus

must possess high adsorptive power for efficient harvesting.


Microcystis aeruginosa

Microcystis aeruginosa

Scenedesmus obliquus

Scenedesmus obliquus
Nannochloropsis sp.

Microalgal harvesting is generally carried out by two types of


Microcystis sp.
Chlorella vulgaris

magnetic particles, naked and surface functionalized. In the case of


C. pyrenoidosa

D. subspicatus
Microalgae

naked magnetic particles, electrostatic interactions between the nega-


tively charged algal cells and positively charged magnetic particles
Table 8

allow the microalgal cells to be harvested [123]. Naked magnetite


synthesized by different methods was found to be successful in

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

Complete demagnetization of cells was


flocculation in the same and different strains respectively [138]. This
shows that genetic modifications may facilitate flocculation to a great
Recovery efficiency of flocculant

extent.

5. Life Cycle Assessment (LCA) and technoeconomic analysis


(TEA) of the harvesting processes

Recently, LCA studies have been carried out by researchers to


achieved

evaluate the impacts of the harvesting processes on the E3 mechanism


∼97%
90%

83%

80%

(energy, economic and environmental). However, the results tend to



fluctuate owing to the different assumptions made about algal culti-


vation procedures, lipid content, processing scale size and application
of end products in these studies. The use of high energy, along with
Process time

high GHG (greenhouse gas) emissions during the dewatering process is


(min)

the main challenge involved during the microalgae harvesting [139]. In


5-10

1-2
10

addition to LCA, TEA is also an integral tool that establishes a capital


2

1

and operating cost profile to determine the economic viability of the


5 mL or 100 m L
Working volume

harvesting technique for its commercial application. However, high


variation in methodology of TEA in literature makes it difficult to draw
50 mL
10 mL

10 mL

10 mL

a conclusion over the economic feasibility of harvesting techniques.


5 mL

5 mL

Based on the economic assessment, researchers found that opera-



tional costs and energy consumption involved during harvesting from


closed cultivation system range below 0.5 €·kg−1 algae and
PDDA = 600 mg L−1; NPs = 20 g

2.5–50 g particles g−1 microalgae

0.5 kWh·kg−1 of algae respectively. However, for an open system the


operational cost and energy consumption increases to 0.3–2.0 €·kg−1
3:1 mass ratio of IOMMs to
1.6 g of dMNF g−1 of cells

algae and 4.5 kWh·kg− 1 algae respectively [29]. For manufacturing


0.46 g particle g−1 cell

high-value products such as nutraceuticals or nutrient supplements


30 g g−1 of cells

from microalgal biomass, centrifugation is the most reliable process.


mass ratios ≥7
Coagulant dose

However, the method is costly owing to its high energy requirement


10 mg mL−1
120 mg L−1

microalgae

[140]. Moreover, dewatering of microalgal biomass by using centrifuge


generates 398.48g CO2 eq per MJ of algae biodiesel, whereas 241.87g
L−1

CO2 eq per MJ of algae biodiesel is generated when filter press is ap-


plied for dewatering [125]. Collotta et al. [141] carried out a com-
Algal concentration

1.3-1.5 g cells L−1

parative LCA using the SimaPro software in order to assess environ-


mental impacts resulting from the use of two microalgal harvesting
Recovery of microalgal biomass by magnetic particle facilitated techniques.

∼2 g L−1

strategies: (a) flocculation followed by centrifugation and (b) direct


0.2 g L−1

1.6 g L−1
0.3 g L−1

centrifugation. Sole centrifugation appeared to be more detrimental for


the environment when compared to the flocculation scenario.

Polyelectrolyte poly(diallyldimethylammonium chloride) (PDDA).

Brentner and colleagues also performed a comparative LCA analysis


Fe3O4-embedded carbon microparticle
Silica-coated magnetic particles called

on three harvesting technologies: centrifugation, filtration and floccu-


Bare-Fe3O4 magnetic particles (bMP)
CTAB-decorated Fe3O4 nanoparticles
dMNF coated with APTES and OTES

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

mental impacts [127]. On the other hand, a study by Granados et al.


[142] found that during flocculation the algal cake is contaminated by
Naked Fe3O4 particles

the flocculants and so it cannot be re-used, and hence it is disposed of in


the environment. Although flocculation exerts a least negative effect on
NPs with PDDA
Flocculant type

the environment, a major impact is afflicted by the choice of flocculant


DEAE MBs

MagSilica

[143]. In contrast, harvesting of microalgal biomass through cen-


IOMMs

trifugation does not require the addition of flocculants, and so the algal
cake is digested anaerobically for energy recovery. During flocculation
Chlamydomonas reinhardtii

process, the cost of operation is significantly increased due to the ad-


Nannochloropsis maritima
Nannochloropsis oceanica

dition of flocculants, such as metals, that may have a negative impact


on the quality of the products or affect the equipment involved in the
Chlorella sp. KR-1

Chlorella sp. KR-1

Chlorella sp. KR-1


Chlorella sp. KR-1
Chlorella vulgaris

Chlorella vulgaris

conversion process [86]. Chitosan can be used as the flocculant as it is


Chlorella sp.
Microalgae

non-toxic, organic and possess the potential to break down in down-


stream operations such as anaerobic digestion. Heasman et al. [49]
Table 9

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

eliminates the use of chemicals to concentrate the microalgal biomass


making the downstream products free of contamination. The medium
can be recycled and reused after the microalgal biomass is harvested
through ultrasonic technology. Coons et al. [148] found that the ul-
trasonic process is environmental-friendly and cost-effective since the
process is capable of meeting both National Alliance for Advanced
Biofuels and Bioproducts (NAABB) and National Algal Biofuels Tech-
nology Roadmap (NABTR) targets as compared to other conventional
methods such as centrifugation, coagulation, flocculation, filtration and
flotation.
The impact of post-harvesting algae concentration on total cost is
detailed in Fig. 3. It was seen that post-harvesting algae concentration is
inversely proportional to the total cost involved. Low investment costs
Fig. 3. Effect of algae concentration after harvesting on the total costs for the along with lower energy consumption by the smaller equipment in the
combination of pressure filtration to 10% dry matter and centrifugal dewa- dewatering step are the possible reasons for reduction in total cost.
tering to 15% dry matter (Adapted from Ref. [29]).
However, reduction in cost was found to be negligible beyond har-
vesting concentration of 50 kg m− 3. Fasaei et al. [29] also concluded
$18/kg according to the information obtained from industrial grade that same trends could be seen for all other harvesting and dewatering
chitosan suppliers [144]. scenarios.
In a harvesting experiment, Aragon et al. [145] found that elec- Detailed LCA and TEA studies for the harvesting techniques dis-
trolytic methods such as electrocoagulation, electroflotation, and elec- cussed in this paper is not available yet. As new harvesting strategies
troflocculation were superior to chemical flocculation as the electrolytic are being developed and very limited data on LCA and TEA are avail-
methods required shorter separation time and is less likely to be con- able (Table 10), these studies need to be carried out to validate the
taminated by metallic hydroxides. Electrolytic methods require low methods for their energy efficiency and overall sustainability.
current strength to attain effective coagulation. Each of the electrolytic
approaches has the potential for scale-up. Although polymeric mem-
6. Conclusions and future prospects
branes are natural candidates for microalgal filtration, membrane
fouling is a major drawback [146]. Research found that ceramic and
Each of the aforementioned techniques works on its own principle,
metallic inorganic membranes are better than polymeric membranes
and so has its own merits. But, till date, there is no specific method or
because of higher water flux and biofouling resistance. In membrane
combination of harvesting methods available for harvesting different
technology, the energy is consumed because of the pressure gradient,
types of microalgae. All harvesting methods concentrate the microalgal
which is generated across the membrane, due to various membrane
biomass to a certain extent, and this concentrated biomass is then
properties. For an assumed pressure gradient, the cost of harvesting is
further dried to extract the desired product. High quality and quantity
found to decrease proportionally with increasing membrane perme-
of microalgal biomass can be recovered without the addition of che-
ability. As compared to the cross-flow filtration cost, the energy con-
micals by using physical harvesting methods. As there are minimal
sumed, and the cost for dewatering the concentrated sludge seems to be
chances of contamination when the biomass is harvested via the pro-
insignificant. Thus, membrane technology has the potential for har-
cesses mentioned above, the extract from the biomass can be used for
vesting with a small level of energy consumption [147]. The application
high-value products. However, physical methods require high operating
of ultrasonic technology for harvesting microalgal biomass has many
cost and time, making the process economically unfeasible. In chemical
advantages over conventional methods. Ultrasonic technology
harvesting methods, the use of chemical flocculants or coagulants

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)

Sedimentation – – 0.05-0.1 kW h m−3 – 2.11-28 [205]


Centrifugation Nannochloris sp. 94-99 0.70-1.30 kW h m−3 US$0.864 L−1 of oil 242 [51]
Flotation – 49.5 0.16-0.44 kW h kg−1 €0.02-0.04 kg−1 57.8-80 [206]
DW
Filtration
PVDF membrane – 98-99 0.91 kW h m−3 – – [207]
PNM membrane Scenedesmus obliquus 94 – US$0.048 kg−1 – [208]
Tangential flow filtration Tetraselmis suecica 89 3.58 kW h kg−1 – 40-45.4 [30]
Inorganic flocculants
Alum – 66-82 – US$0.4-2.1 kg−1 1.26-36 [175]
Organic flocculants
−1
Chitosan Scenedesmus sp. 92 – €2-100 kg 8.88-56 [175]
Organic polymer Scenedesmus sp. 80 36.81 kW h kg−1 – – [30]
Autoflocculation
pH modification Chlorella vulgaris, Scenedesmus sp., 90 0.02–0.2 kW h m−3 US$0.13 kg−1 10 [80]
Chlorococcum sp.
Electrical based harvesting
Electrochemical (non-sacrificing carbon Chlorella sorokiniana 94.52 1.6 kW h kg−1 – – [209]
electrode)
Electrocoagulation-flocculation (Al and – 90 2 kW h kg−1 – 47.9 [23]
Fe electrodes)
Electrocoagulation (polarity exchange) Nannochloris oculata 90 1.08 kW h kg−1 – – [210]
Magnetic particle assisted harvesting Botryococcus braunii 98 6.5 kW h m−3 – 65 [125,149]

14
M. Roy and K. Mohanty Algal Research 44 (2019) 101683

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