Algal Research 47 (2020) 101841

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

Review article

A review on microalgal culture to treat anaerobic digestate food waste T

effluent
David Chuka-ogwudea,b, James Ogbonnab, Navid R. Moheimania,c,
⁎

a
Algae R & D Centre, Environmental and Conservation Sciences, Murdoch University, College of Science, Health, Engineering and Education School, 90 South Street,
Murdoch, WA 6150, Australia
b
Department of Microbiology, University of Nigeria, 410001 Nsukka, Enugu State, Nigeria
c
Centre for Sustainable Aquatic Ecosystems, Harry Butler Institute, Murdoch University, 6150, Australia

ARTICLE INFO ABSTRACT

Keywords: Food waste constitutes a significant portion of waste in the world. Indeed, it is estimated that about one-third of
Raceway ponds edible human food is wasted globally. Anaerobic digestion has been identified as a promising technology for the
Inclined ponds treatment of food waste as it generates a significant amount of energy and can remove a substantial portion of
Closed photobioreactors the organics. However, this process has not been adequately applied due to technical and economic challenges.
Algae
Most importantly, anaerobic digestion of food waste produces waste in the form of Anaerobic digestate food
Anaerobic digestate effluent
effluent (ADFE), with high amounts of nutrient such as ammonium (up to 3000 mg L−1 NH3-N). It has been
established that this effluent can be used as a substrate for the cultivation of microalgae allowing both a means of
its treatment and its possible valorization. This paper reviews the anaerobic digestion of food waste, the com-
position of its digestate and trends in the treatment of ADFE with emphasis on treatment using microalgae.
Potential microalgal cultivation methods applicable to the treatment of anaerobic digestate, especially ADFE,
and possible optimization of the cultivation methods are also reviewed critically. Further, understanding of the
cultivation of microalgae in ADFE is required to aid in better design of its treatment process and valorization to
improve its economics.

1. Introduction
The exponential growth of the human population over the years has
been accompanied by a range of problems, including the significant
growth of waste emanating from the activities of the population.
According to the Food and Agricultural Organization (FAO), roughly
one-third (about 1.3 billion tons) of the edible parts of food produced
for human consumption, gets lost or wasted globally per year [1]. The
amount of food waste generated has been projected to increase sig-
nificantly in the next 25 years due to economic and population growth,
especially in Asian countries [2]. About 1.4 billion hectares of the
earth's fertile land, (28% of the worlds agricultural area) is used to
produce food that is wasted or lost. The carbon footprint of food waste
is estimated to contribute to greenhouse gas (GHG) emissions up to 3.6
GT/year (gigatons) of CO2 equivalent [1–3].
It is challenging to know the exact content and composition of food
waste because of its heterogeneous nature born from the heterogenicity
of its sources; which is strongly related to the eating habits of the
populace of the environment from which it is sourced. Total solid (TS)
and volatile solid (VS) contents are in the ranges of 18.1–30.9 and
17.1–26.35, respectively, indicating that water accounts for 70–80% in
food waste. Conventionally, food waste, which is a component of mu-
nicipal solid waste, is incinerated or dumped in open areas or pits,
which may lead to severe health and environmental problems [4].
Landfilling and incineration lead to an undesired increase in carbon
footprint by the release of significant amounts of methane gas and CO2,
respectively [5]. Leachate from landfills can also lead to ground-water
pollution and consequently, pollution of nearby waterways [4]. In ad-
dition to the undesired carbon footprint of food waste on the environ-
ment, incineration of food waste consisting of high moisture content is
highly energy-intensive and results in the release of dioxins (poly-
chlorinated dibenzo-p-dioxins (PCDDs), polychlorinated dibenzofurans
(PCDFs), and coplanar polychlorinated biphenyls (PCBs)) [2,6]. Ex-
haust gases from food waste incinerators may contain significant
amounts of dioxins formed from chlorine-containing compounds found
in food samples [7].

⁎
Corresponding author at: Algae R & D Centre, Environmental and Conservation Sciences, Murdoch University, College of Science, Health, Engineering and
Education School, 90 South Street, Murdoch, WA 6150, Australia
E-mail address: n.moheimani@murdoch.edu.au (N.R. Moheimani).

https://doi.org/10.1016/j.algal.2020.101841
Received 15 August 2019; Received in revised form 29 January 2020; Accepted 11 February 2020
Available online 20 February 2020
2211-9264/ © 2020 Elsevier B.V. All rights reserved.
D. Chuka-ogwude, et al. Algal Research 47 (2020) 101841

Here, we review the anaerobic digestion (AD) process as a way of Table 1

treating the organic food wastes. However, anaerobic digestion is an Methane Yield from various waste substrates and some algal biomass.
incomplete process. Anaerobic digestion converts the organics to me- Waste substrate Methane yield (L g−1 VS Reference
thane and CO2, but the AD effluent contains a high content of inorganic feed)
nitrogen and phosphates. Microalgae cultivation as a potential way to
Maize silage 183 ± 10.1 [21]
treat such effluent is reviewed critically.
Swine and cattle manure 205 ± 3.7 [21]
Dairy wastewater 241 ± 5.5 [21]
2. Anaerobic digestion of food waste Wastewater sludge 267 ± 10.9 [21]
Fruit and vegetable waste 160–350 [17]
The high nutrient content of food waste suggests the potential for Municipal solid waste 186–222 [22]
Slaughter house waste + organic fraction 400–500 [23]
energy recovery through biochemical or thermochemical means
of municipal waste
[2,8–11]. Anaerobic digestion, which is widely deployed and reason- Yard waste 134–209 [22]
ably understood, is a biochemical treatment that favors high moisture Food waste 540 [24]
biomass such as food waste and has been proposed as a cost-effective Kitchen food waste 446 [25]
Municipal food waste 472 [26]
technology for the recovery of energy/renewable energy production
Source segregated food waste 402 [9]
from food waste [12]. Chlorella sorokiniana 220–280 [27]
Spirulina maxima 250–340 [28]
2.1. Anaerobic digestion Euglena gracilis 458 [29]
Nannochloropsis oculate 204 [30]
Chroococcus sp 317 [31]
Anaerobic digestion is the natural, biological degradation of organic
matter, in the absence of oxygen, to biogas. Biogas is constituted of
60–70% methane and 30–40% carbon dioxide and traces of other gases alleviate the cost. Also, it has been shown that food waste as a substrate
[13]. The benefits of anaerobic digestion include renewable energy has the potential to provide higher biogas yield (Table 2) in comparison
generation in the form of bio-methane, reduction in greenhouse gas to cow manure, pig manure, corn silage, and so forth [19].
emission, and the potential revenue stream from AD waste such as There are reports on anaerobic digestion of source-segregated do-
fertilizers, bio-oil, syngas, biochar, ethanol, electricity, hydroponics, mestic food waste (Table 1) and interest is growing in this area within
fiber for animal bedding and algal biomass [11]. Europe due to rising energy costs associated with the processing of wet
Anaerobic digestion consists mainly of four phases: enzymatic hy- waste, the requirement to meet the diversion targets of the EU Landfill
drolysis, acidogenesis (acid formation), acetogenesis, and methano- Directive (99/31/EC), and the need to comply with regulations for the
genesis (gas production). Enzymatic hydrolysis involves the breaking disposal of animal by-products (EC 1774/2002) [9]. Currently, the
down of large polymers that otherwise cannot be transported into the economic prospects for food waste collection and anaerobic digestion
cell membranes, by hydrolases secreted by facultative or obligate programs are poor [20], and factors like Feed-in tariffs (FiTs) (subsidies
anaerobic bacteria (Streptococcus and Enterococcus). Polysaccharides are paid to producers of certain energy sources) and further product ex-
broken down into oligosaccharides and monosaccharides. Proteins are traction/valorization of anaerobic digestate effluents are beneficial for
broken down to amino acids and peptides, and lipids are broken down future anaerobic digestion development.
into glycerol and fatty acids [2]. In the acidogenesis phase, products
from the hydrolytic phase are fermented to volatile fatty acids such as
acetate, butyrate, valerate, propionate and isobutyrate along with 2.3. Characteristics of ADFE
carbon dioxide, ammonia and hydrogen by facultative anaerobic bac-
teria (Ruminococcus, Paenibacillus, and Clostridium species). This utilizes Table 2 details various features of food waste digestate, highlighting
oxygen and carbon thereby creating anaerobic conditions for metha- important constituents, obtained from multiple sources, and also other
nogenesis [2]. In acetogenesis phase, the volatile fatty acids from the sources of digestate for comparison. Raw anaerobic digestate food ef-
hydrolysis phase products are converted into acetate and hydrogen by fluent (ADFE), withdrawn from digesters, is a liquid to a thick slurry
acetogenic bacteria of the genera Syntrophomonas and Syntrophobacter that contains a significant quantity of solids. ADFE composition varies
[14]. In methanogenesis phase, methane is produced either by the depending on the composition of the feedstock, source of inoculum,
fermentation of acetic acid or the reduction of carbon dioxide from the digester operating conditions (pH, temperature, organic loading rate,
acetogenesis phase. Acetoclastic methanogens, belonging to Archaea, hydraulic retention time) and anaerobic digester configurations [42].
produce methane from acetic acid and hydrogenotrophic methanogens The characteristic of the digestate also depends on what part of it is
produce methane via the reduction of carbon dioxide by hydrogen. used. Digestate could be used whole or separated into two parts: solid
About 30% of methane in methanogenesis is produced from the re- digestate, containing most of the insoluble portion of the total solids
duction of carbon dioxide, while 70% is from the splitting of acetic acid (TS) and liquid digestate, containing most of the Volatile Solids (VS) of
[15,16]. Examples of methanogens include Methanosaeta, Methanolobus, the TS. ADFE contains similar amounts of total ammonia nitrogen
Methanococcoides, Methanohalophilus, Methanosalsus and Methanohalo- (TAN) with cattle and piggery slurry digestate but higher total am-
bium species. monia nitrogen content than dairy waste and wastewater sludge
anaerobic digestate. The range of total ammonia nitrogen in different
2.2. Application of anaerobic digestion for treatment of food waste sources of ADFE is wide (800–6000 mg L−1), but it could be said that it
is generally higher than found in other digestates. The ratio of nitrogen
Anaerobic digestion is a mature and widely applied technology in to phosphorus (N/P) in ADFE is generally higher than Anaerobic di-
the treatment of high-strength wastewater, sewage sludge, and animal gestate effluents from other sources (see Table 2).
manure. However, adopting it for food waste treatment/management ADFE pH generally ranges from 6.7 to 8.4 [43] due to degradation
still faces technical challenges such as volatile fatty acid accumulation, of volatile fatty acids and the production of ammonia during the process
process instability, high foaming, low buffer capacity and economic of digestion. The increase in pH and NH4+eN content through anae-
challenges such as high cost of transportation and operation [17]. In- robic digestion enhances the polluting potential of the digestate during
deed, < 2% of US food waste is anaerobically digested [18]. Thus, it is storage [44] as well as during land spreading [45]. The pH of the di-
expedient to identify current challenges in the process to improve ef- gestate also affects the solubility of phosphate (PO4−3). Higher pH
ficiency and identify the potential for further product extraction to (> 10) causes phosphate precipitation into calcium or magnesium

2
D. Chuka-ogwude, et al. Algal Research 47 (2020) 101841

phosphates (Ca3(PO4)2 or Mg3(PO4)2) and struvite (NH4MgPO4.6H2O),

Reference
a complex crystal that contains nitrogen, phosphorus, and magnesium.
[32]
[21]
[21]
[21]
[21]
[33]
[34]
[35]
[36]
[37]
[38]
[39]
[40]
[41]
Lower pH increases the solubility of phosphates [46]. Undiluted ADFE
application as a substrate for microalgae propagation is limited due to
the toxicity of high ammonia concentrations to the algal biomass [47].

615 ± 64.8
1045 ± 55

Furthermore, high pH can result in a significant amount of ammonia

not being assimilated but lost to the atmosphere during its use as a
–
–
–
–
–
–
–
–
–

–
–
–
substrate for algae cultivation [48]. The main concerns regarding the
VS

further application of digestate are emissions of ammonia to the en-

vironment through ammonia (NH3) volatilization, nitrate (NO3−)
1225 ± 125

705 ± 21.2
leaching and greenhouse gas emissions as nitrous oxide (N2O), with
Properties of various Anaerobic Digestate Effluents. Total solids (TS), volatile solids (VS), Chemical Oxygen Demand (COD), total nitrogen (TN). All units (except pH) are in mg L-1.

20,000
1040

associated impacts on air and water quality, ecosystem functioning and

–
–
–
–

–
–
–

–
–
–
human health [49].
TS

2.4. ADFE treatment processes

8.31 ± 0.1
6.9 ± 0.3

8.3 ± 0.4
6.8 + 0.4
7 ± 0.1

7 ± 0.3

7.9–8.0
7.82

7.5
8.5

8.3

The challenges involved in the treatment and reuse of anaerobic

–

–
–

digestate effluents is a likely cause for the under-utilization of anaerobic

pH

digestion [50]. Table 3 summarizes the emerging trends for the man-
agement of liquid digestate, which include: Anaerobic ammonium
28.14 ± 0.11
11.69 ± 0.1
10.9 ± 2.5
31 ± 3.4
29 ± 4.9
74 ± 5.7
61 ± 7.4

oxidation (ANAMMOX), ammonia stripping, reverse osmosis, struvite

47.8
432
140

44

crystallization, constructed wetlands, hydroponics and algae cultiva-

–

tion. These processes aim at drastically reducing, to completely re-

TP

moving the nutrients in the digestate, leaving close to ‘clean water.’ The
water obtained at the end of these processes could be used for irrigation
216.3 ± 14.2

in areas of drought, as animal drinking water, and as a form of process

14.0 ± 2.7
12.6 ± 2.5
10.4 ± 1.8
10.8 ± 2.0
4.9 ± 7.4

35 ± 3.8

water in several industries. Table 3 also summarizes some of the pros

227
–
–

–
–

and cons of the processes mentioned above. The most common method
PO4

for the reuse of anaerobic digestate has been land application for crop
production because large quantities can be spread over large areas of
farmland [51]. However, improper land application may lead to am-
107.0 ± 61.9
0.24 ± 0.02
12.5 ± 6.4

19 ± 3.0

monia volatilization, pathogen contamination, over-fertilization, and

–
–
–
–
–
–

–
–

–
–

nutrient runoff, causing reasonable concern regarding the environ-

NO3

mental sustainability of the process [51]. Trends employed for the

management of the solid fraction (solid digestate) include: composting
and newer trends like pyrolysis for the production of syngas, bio-oil,
2814.97 ± 53.67
1280.97 ± 20

and biochar [52]. Fibers and insoluble solids from solid digestate can
805.1 ± 18.2

1400 ± 210
1160 ± 90
460 ± 26
596 ± 77

also be effectively reused for the production of particleboard and bed-

1770
1240

2370

1400
–

ding materials [64,65].

As highlighted in Table 3, algae treatment of digestate including
TN

ADFE, is potentially the most efficient means mainly because of va-

lorization of digestate through the broad scope available for the ap-
plication of microalgal biomass. Microalgae cultivation systems can
2213.54 ± 47.77
5226.0 ± 115.9
1172.38 ± 25
802.1 ± 20.3

1150 ± 180

1300 ± 41

also run as ‘standalone’ systems without the need for complex in-
410 ± 38
470 ± 46

910 ± 77
1510
1200

3700

2120

tegration of other supporting systems. Also, microalgal cultivation can

-`

easily be integrated into the process flow of anaerobic digestion sys-

TAN

tems, creating a closed loop.

3. Microalgae culture to treat ADFE

6096.10 ± 40.66
1856.6 ± 118
3300 ± 270

7800 ± 390
6200 ± 430

6096 ± 34

1600 ± 12
920 ± 62

3.1. Microalgae and AD treatment

2290
1980

1500
5923

3180
–

Microalgae are sunlight powered cell factories that can fix CO2
COD

converting it into biomass that can produce valuable lipids, carbohy-

drates, proteins, pigments, and vitamins [66]. These products can then
Pig excrement & kitchen garbage ADE

be converted into biofuels, feeds, foods, and high-value bio-compounds.

Maize silage & Swine manure ADE

Microalgae are a very diverse group of organisms, they do not require

Food waste anaerobic Digestate

Food waste anaerobic digestate

Food waste anaerobic digestate

arable land for cultivation and they tolerate and grow on a variety of
nutrient sources and several types of wastewater [67,68]. The nutrients
Food wastewater Digestate
Piggery wastewater ADE
Wastewater Sludge ADE

and water needed for the cultivation of microalgae are readily available
Piggery effluent ADE

in wastewater streams and utilizing wastewater will allow for sig-

Cattle manure ADE

Kitchen waste ADE

Kitchen waste ADE

Dairy waste ADE
Food waste ADE

nificant cost cuts for microalgae cultivation while simultaneously

treating the wastewater to acceptable levels [69].
Anaerobic digestate effluent offers all the same benefits expected
Table 2

Source

from wastewater treatment using microalgae. The drawback of its

usage, as stated earlier, is in its “strength” (toxic concentrations of

3
D. Chuka-ogwude, et al.
Table 3
Trends in the management of Anaerobic Digestate Effluents; Some pros and cons.
Method Pros
Anaerobic ammonium oxidation i. Low energy, oxygen and carbon requirements
(Anammox) ii. Consumes atmospheric CO2 reducing
greenhouse gases.
Adsorption i. Efficient on large scale application
Constructed wetlands i. Relatively low set-up cost
ii. Operational simplicity
Phycoremediation i. Anaerobic digestate effluent can substitute for
fertilizer requirements of algae.
ii. Algal biomass produced may be further
valorized in feed or bio-fuel production.
iii. Can be used as a standalone treatment.
Ammonia Stripping i. Easy In-situ application.
ii. Highly efficient for ammonia removal.
Reverse osmosis Suitable for heat-sensitive substrates, low
operating cost.
Struvite Crystallization i. Recovery of high-quality fertilizer in the form
of struvite.
ii. Pellets are easy to handle.
Hydroponics i. Can be used as a standalone treatment
ii. Easy to accomplish
iii. Nutrient valorization
nutrients) and high turbidity. Significant work has been carried out on
the use of anaerobic digestate from various sources, for the cultivation
of microalgae with varying degrees of success as depicted in Table 4.
Nitrogen and phosphate removal are the most important parameters in
the treatment of any wastewater/effluent and microalgae has proven to
be efficient in the utilization of these nutrients for growth in cultivation.
Table 4 highlights extensively the nutrient removal rate (COD, phos-
phates and Nitrogen) and efficiency from various studies. Microalgae
cultivation has been demonstrated to reduce the COD of waste effluents
and digestates to up to 90% (see Table 4). Degradation of organic
compounds in anaerobic digestate can be attributed to mixotrophic
growth in microalgae and for the purpose of organic pollutant de-
gradation, mixotrophs employing osmotrophy for organic carbon have
been alluded as significantly relevant [70].
Microalgae capable of mixotrophy are generally able to reach sig-
nificantly higher cell densities in culture than strict photoautotrophs
[71–74] and so would naturally be the preferred choice for treatment
and valorization of waste effluents with complex compositions and high
COD like ADFE. For some mixotrophic microalgae, oxidative phos-
phorylation of organic carbon sources and photosynthesis seem to
function in parallel and additively, with mixotrophic growth rates
equaling or even surpassing the sum of heterotrophic and autotrophic
growth of the microalgae [75]. In other cases, organic carbon utiliza-
tion may reduce affinity for CO2 and CO2 fixation, and suppress pho-
tosynthetic oxygen evolution [76]. The utilization of organic carbon has
also been shown to cause strong inhibition of the Calvin cycle enzyme
ribulose bisphosphate carboxylase/oxygenase (RuBPCase) [77], and the
down-regulation of RUBISCO activase and genes responsible for
synthesis of various light harvesting proteins; including reduced
chlorophyll ‘a’ content per cell [71]. Under mixotrophic conditions net
maximum photosynthetic O2 evolution rate, saturation irradiance (Ik)
and variable to maximum chlorophyll fluorescence ratio (Fv/Fm) have
been shown to be depressed indicating reduced photochemical effi-
ciency of PS II [72]. In some exceptional cases however, mixotrophic
conditions can increase photosynthetic rate and PSII photochemical
efficiency [78]. Nevertheless, whichever response is observed, the
consensus is that for most species, biomass growth and productivity of
4
Algal Research 47 (2020) 101841
Cons References
i. Slow growth rate of Anammox organisms leading to prolonged [53]
start-up times.
ii. Water consumption increasing capital cost, for dilution of
digestate toxic concentrations of Nitrogen in digester inhibit
biomass.
iii. Cannot be used as a standalone treatment.
i. High initial investment costs [54]
ii. Difficulty in the removal of adsorbed nutrients / colloids from the
adsorbents
iii. After use disposal safety concerns
i. Requires large surface area [55]
i. Can consume a significant amount of water if diluted, leading to [35,48,56,57]
high operational cost.
ii. Requires large surface area
i. Ammonia gas fouling, [58,59]
ii. Ammonia gas release (greenhouse gas release)
iii. Requires high temperature and pH
The process requires a lot of water, which may remove desired [60,61]
nutrients.
i. High costs of chemical compounds [62]
ii. Cannot be used as a standalone treatment.
i. Requires dilution. [63]
ii. Potential concerns regarding plant contamination by digestate
bacteria.
microalgae is improved under mixotrophic conditions.
Other issues to consider in the treatment of anaerobic digestates
using microalgae is the organic content and microbial load of the ef-
fluent and the products that are to be obtained from the microalgal cells
after treatment and valorization using microalgae. The dynamics of the
relationship between microalgae and bacteria in anaerobic digestates
can get quite complex because of the diversity of the organisms in di-
gestates. These relationships range from mutualism to commensalism to
parasitism [79]. Ultimately, microalgae have been shown to out-
compete bacteria, including nitrifying bacteria, for nutrients especially
under phosphate limiting conditions [80]. In general, environmental
conditions of algal cultivation systems, such as variable pH, high light,
high dissolved oxygen and shear produced by mixing, has been found to
limit the survival (up to 99%) of many pathogenic bacteria such as
coliforms and Salmonella [81].
All the studies on the cultivation of microalgae on anaerobic di-
gestate highlight nutrient toxicity and turbidity as the major constraints
and various pre-treatment procedures are employed before its usage
(Table 4). The challenges, common attempts to ameliorate the said
problems and potential solutions are discussed in the following sec-
tions.
3.2. Challenges of using AD effluent for algal growth
3.2.1. Turbidity
Turbidity is one of the most prominent challenges experienced in
the use of microalgae to treat AD effluent [33,57]. Regardless of the
cultivation system, light (quantity and quality) is the main limiting
factor of any microalgae culture. Photosynthesis correlates with an in-
crease in irradiance until maximum algal growth is achieved at the light
saturation point [105,106]. Suspended materials in anaerobic digestate
effluent interfere with the clarity of the liquid medium and greatly in-
creases light attenuation because the light is scattered and absorbed by
the suspended materials [57]. Impurities responsible for turbidity in-
clude clay, silt, finely divided organic and inorganic matter, soluble
colored organic compounds, and microorganisms. Turbidity has been
tackled by researchers by pre-treatment of the anaerobic digestate
D. Chuka-ogwude, et al. Algal Research 47 (2020) 101841

Table 4
Microalgae cultivation on Anaerobic Digestates. System of cultivation, productivities and nutrient removal efficiencies.
Algae species Digestate Digestate Pre- Cultivation System Operation Biomass Productivity Nutrient Reference
Origin treatment and Concentration Removal
Efficiency

Chlorella pyrenoidosa Starch Filtration, 2 L flasks Batch (9 d) 0.58 g/L/d TN 91.6% [82]
processing Sterilization, 3.01 g/L TP 90.7%
wastewater Dilution with COD 75.8%
wastewater
C. pyrenoidosa Starch Precipitation, Airlift circulation Outdoor batch 0.37 ± 0.09 g/L/d TN 83.1% [83]
processing Filtration photobioreactor (14 d) sparging 2.05 g/L TP 97.0%
wastewater (890 L) with 5–9% CO2 COD 66.0%
Chlorella PY-ZU1 (Mutated) Swine manure Undiluted, Benchtop column Batch sparging 0.601 g/L/d TAN 73% [84]
and sewage Centrifugation, bioreactor (0.3 L) with 15% CO2 4.81 g/L TP 95%
Autoclave COD 79%
Chlorella PY-ZU1 Food waste Undiluted, 1 L Flasks Batch sparging 0.456 g/L/d,4.3 g/L TAN 99% [40]
Ozonation, with 15% CO2 TP 99%
Autoclave COD 68%
Chlorella sp. Dairy manure Dilution, Filtration 250 mL Flasks Batch (21 d) 1.71 g/L TN 82.5% [57]
TAN 100%
TP 74.5%
COD 38.4%
Chlorella sp. Biogas Fluid Ultraviolet, Photobioreactor bag Batch (6 d) with 0.494 g/L TN 73.1% [85]
(slurry) Filtration (40 L, Effective 8 L) biogas in TP 67.6%
headspace COD 78.9%
Chlorella sp. Wastewater Centrifugation Glass cylinders (0.38 L) Batch (until 0.45 g/L/d TN 83.7% [86]
sludge stationary phase) 2.11 g/L TP 94.2%
COD 86.3%
Chlorella vulgaris Dairy manure Dilution Flask (4 L, effective Semi continuous 1.3 g/L TN 93.6% [87]
1 L) (30 d) with 2% TAN 100%
CO2 TP 89.2%
COD 55.4%
Chlorella minutissima, Poultry litter Centrifugation, 0.25 L Flasks Batch (12 d) 0.076 g/L/d TN 60% [88]
Chlorella sorokiniana Dilution 0.612 g/L TP 80%
and Scenedesmus
bijuga
C. vulgaris, Scenedesmus Livestock waste Ultraviolet, Photobioreactor bag Batch (7 d) with – TN 76.0% [89]
obliquus, and Neochloris (Biogas slurry) Filtration (20 L, Effective 4 L) biogas in TP 63.2%
oleoabundans headspace COD 63.1%
CO2 62%
C. vulgaris and nitrifying – Vinasse Dilution HRAP 180 L Continuous (175 11.8 g/m2/d TN 37% [90]
denitrifying activated sludge d) with synthetic 0.6 g/L TP 71%
biogas sparging COD 51%
TOC 57%
TIC 78%
CO2 80%
C. vulgaris, N. oleoabundans, Cattle slurry Dilution 250 mL Flasks Batch (21 d) in 0.26 g/L/d TAN 99.9% [91]
and S. obliquus and raw cheese CO2 incubator PO4-P 97.3%
whey
Chroococcus sp. Algae cells Dilution / mixed Transparent Plastic Batch (12 d) with 1.42 g/L TAN 85.2% [92]
with wastewater bottles 20 L air sparging NO3-N 77.3%
TP 89.3%
COD 70%
Desmodesmus sp. Pig manure Filtration, Dilution 1 L Flasks Batch (10 d) 0.385 g/L TN 75.6% [93]
TAN 92.7%
PO4-P 100%
Desmodesmus sp. Pig manure Filtration, Dilution 1 L Flasks Fed-batch (40 d) 1.039 g/L TN 94.2% [93]
TAN 91.1%
PO4-P 88.7%
Desmodesmus sp. Pig manure Filtration, Dilution 100 mL Flasks Batch (14 d) 0.029 g/L/d TN 100% [94]
0.412 g/L TP 100%
Nannochloropsis salina Municipal Dilution with Lab-scale bioreactor/ Batch (10 d) with 0.092 g/L/d TN 100% [95]
wastewater artificial seawater glass bottle (2 L) air sparging 0.92 g/L TP 100%
Nannochloropsis salina Municipal Dilution with Lab-scale bioreactor/ Semi-continuous 0.155 g/L/d TN 89% [95]
wastewater artificial seawater glass bottle (2 L) (18 d) with air TP 82.8%
sparging
Synechocystis sp. Municipal Dilution with Lab-scale bioreactor/ Batch (18 d) with 0.151 g/L/d TN 100% [96]
wastewater artificial seawater glass bottle (2 L) air sparging TP 100%
Synechocystis sp. Municipal Dilution with Lab-scale bioreactor/ Semi-continuous 0.212 g/L/d TN 100% [96]
wastewater artificial seawater glass bottle (2 L) (18 d) with air TP 100%
sparging
N. oleoabundans Dairy manure Dilution Indoor photobioreactor Batch (11 d) with 0.088 g/L/d TAN 90–95% [97]
(polyethylene tubing 2–3% CO2
(U-Line)) 50 L sparging
Scenedesmus accuminatus Livestock waste Filtration, cylindrical glass Semi-continuous 0.118 g/L/d, 1.5 g/L TN 89% [34]
Autoclave, Dilution reactor (1 L) (29 d) with air
sparging
(continued on next page)

5
D. Chuka-ogwude, et al. Algal Research 47 (2020) 101841

Table 4 (continued)

Algae species Digestate Digestate Pre- Cultivation System Operation Biomass Productivity Nutrient Reference
Origin treatment and Concentration Removal
Efficiency

Scenedesmus sp. Swine manure Autoclave, Mixed Indoor photobioreactor Batch then 0.67 g/L/d TAN > 95% [98]
with municipal (1.8 L) continuous PO4-P > 97%
wastewater chemostats (45 d)
with air sparging
S. obliquus Livestock waste Filtration, Photobioreactor bags Batch (7 d) with 0.311 g/L/d TN 74.6% [99]
Autoclave, Dilution (polyethylene, 48 L) biogas in TP 88.8%
headspace COD 75.3%
CO2 73.8%
Mixed microalgae dominated by Wastewater Dilution 0.5 L flasks Batch (7 d) 2.6 g/L TSS – [100]
Scenedesmus sp.
8
Tetraselmis sp. Tetraselmis Dilution Plastic bag Batch (10 d) with 5*10 cells/L – [101]
culture effluent photobioreactors (5 L) air sparging
Scenedesmus bijuga food Dilution, Autoclave 1 L Flask Batch (28d) 0.0508 g/L/d, 1.49 g/L TN 86.6%, TP [37]
wastewater 90.5%
effluent
Chlorella SDEC-18 Kitchen Waste Dilution, I L Flask Batch 0.53 g/L TN 35.21%, TP [39]
centrifugation 95.27%
Scenedesmus dimorphus Diluted food Dilution Indoor Raceway Pond Batch 0.042 g/L/d 65–72% TAN, [102]
waste & animal (100L) 63–100% TP
manure
Chlorella, Scenedesmus, penate Piggery Effluent Sand filtered but Raceway Pond (150 L) Semi-continuous 0.017–0.02 g/L/d – [48]
diatom consortium undiluted with CO2
sparging
Chlorella, Scenedesmus, penate Piggery Effluent Sand filtered but Raceway Pond (160 L) Semi-continuous 0.024 g/L/d – [103]
diatom consortium undiluted
Chlorella, Scenedesmus, penate Piggery Effluent Sand filtered but Biocoil (40 L) Semi-continuous 0.047 g/L/d – [103]
diatom consortium undiluted
Chlorella, Scenedesmus, penate Piggery Effluent Sand filtered and Inclined Thin layer Semi-continuous 0.06 g/L/d, 0.84 g/L 98.06 ± 1.13 [41])
diatom consortium Dilution pond (350 L)
Chlorella, Scenedesmus, penate Piggery Effluent Sand filtered and Raceway Pond Semi-continuous 0.03 g/L/d, 0.84 g/L 98.06 ± 1.13 [41]
diatom consortium Dilution (1500 L)
2
Rhizoclonium, hieroglyphicum, Dairy manure Dilution Biofilm (Algal turf Continuous 25 g/m /d 70–100%TAN &P [104]
Microsporaconsortium scrubber raceway)
(1500 L)

effluent by centrifugation [84,107], filtration [82], precipitation [83]
and adsorption [54] (See Table 3) to remove suspended solids and
impurities. However, the most popular method employed to reduce
turbidity is dilution. There is ample literature that supports better algae
performance, in terms of growth and nutrient removal in anaerobic
digestate effluent due to reduced turbidity [32,35,57,80,100,107].
However, most of these methods are not attractive as they can result in
a significant increase in the cost of the treatment process [84]. See
Table 3 for pros and cons of the aforementioned treatment methods.
3.2.2. Ammonia/ammonium toxicity
Another major problem with the use of anaerobic digestate effluent
for the cultivation of microalgae is the high concentration of nutrients,
especially Ammonia‑nitrogen [48,103]. It has been established that
ammonium is the most preferred source of nitrogen for microalgae
[108–112], but high concentrations are toxic to microalgae. In practice,
as regards to wastewater (including ADFE), ammonium exists alongside
the more reactive ammonia species and is collectively referred to as
ammonia nitrogen. In aqueous solutions, ammonia-N is present in two
forms: the protonated cation NH4+ (ammonium), and the gaseous form
NH3 (ammonia). The equilibrium of the two forms is dictated by pH. At
pH > 9 ammonia dominates and at pH < 8 ammonium dominates. At
pH > 9 toxicity is most likely due to ammonia and at pH < 8 toxicity
is most likely due to ammonium. In algae, ammonium does not diffuse
through the cell membrane; hence, its uptake needs to be regulated. On
the other hand, ammonia diffuses passively through the cell membrane
and hence, cannot be regulated, resulting in high ammonia con-
centrations in the cell [113]. Ammonia is the more reactive species and
is also more toxic to microalgae. The toxicity of ammonia to algae has
been shown to include: the disruption/inhibition of photosynthesis by
damaging the manganese (Mn) cluster of the Oxygen-evolution
complex of photosystem II (PSII) and also increasing the sensitivity of
PSII to photodamage [114]. Also, high ammonium concentrations in-
hibit microalgae photosynthesis by uncoupling electron transport from
photophosphorylation [115,116]. It is also suggested, at least in higher
plants, that using ammonium as the sole nitrogen source can lead to the
oxidation of excess redox equivalents on the mitochondrial electron
transport chain leading to electron ‘leakage’ and the production of re-
active oxygen species (ROS) [117].
ADFE, has a concentration of NH3-N in the range of
1000–6000 mg L−1 [35] and high ammonia-N levels above
100 mg L−1has been shown to have inhibitory effects on the growth of
microalgae in anaerobic digestate effluent [21,34,47,100]. In anaerobic
digestate effluent characteristically with high concentrations of am-
moniacal nitrogen, ammonia volatilization has also been noted to be a
problem in its use as a growth medium [48]. To alleviate the inhibitory
effects of high nutrient concentrations in algal cultures, researchers
again turn to dilution to bring the ammonia-N level to 50–100 mg L-1
[32,47,100].
3.2.3. Nutrient ratios
ADFE and other digestate effluents are characterized by low carbon
to nitrogen, ratios due to the enhanced microbial degradation of or-
ganic matter and the resultant emission of carbon as methane in the
process of anaerobic digestion [118]. It has been shown that the C/N
ratio has a significant effect on biomass production in algal cultures
[119], with higher C/N ratios producing higher biomass. Anaerobic
digestate effluent has been found to have C/N ratios as low as 1.53 [21]
whereas the optimal C/N ratio for algal growth is in the range of 4–8
[120]. However, the addition of CO2 sourced from flue gas or other
sources otherwise considered as waste or pollutants can potentially
solve this issue. Having said that, it should be noted that flue gas also

6
D. Chuka-ogwude, et al.
contain Nitrous and Sulphur oxides (NOx and SOx) [121,122] and these
oxides have been demonstrated to be toxic to microalgal growth
[123,124] so care should be taken to reduce their concentrations to
acceptable levels by treatment. N/P ratio of ADFE is also evidently
much higher than ideal (in extreme cases up to 80). The ideal range is
14–16 [125,126], reflecting nitrogen excess in the form of ammonia.
However, as stated earlier, the composition of the digestate is entirely
subjective to the feedstock of the digestion process and the source of the
digestate. This issue can be resolved by either modifying the feedstock
of the anaerobic process to better suit the use of treating and valorizing
its digestate or using mixed sources of digestate or mixtures of diges-
tates and other wastewater (to complement for nutrient insufficiencies
[82]) for the cultivation of the microalgae.
3.3. Current solutions for treating AD effluents using microalgae
3.3.1. Addition of carbon oxide
Carbon dioxide can play a dual role in the optimization of the
process for the use of anaerobic digestate effluent in the cultivation of
microalgae. Its addition can increase biomass and regulate pH [119].
This will also reduce the need for the use of acid, alkaline, or buffer for
the same purpose. In open-air, when CO2 dissolves in culture medium it
forms carbonic acid (H2CO3) and consequently reduces the pH of the
medium, but when microalgae biomass increases and the rate of pho-
tosynthesis increases, the CO2 is consumed from the medium which
then returns to alkaline pH [68,127]. This is observed as higher pH
levels in the night and lower pH levels in the daylight in algal cultures.
Adequately controlled addition of CO2 could reduce the pH of digestate
to levels that allow for significant biomass improvement and ammonia
solubilization, improving/increasing the amount of nitrogen absorbed
by the microalgae as opposed to that lost to volatilization [48].
Currently, there is no literature on the influence of CO2 addition in
the cultivation of microalgae on ADFE. The impact of the addition of
CO2, keeping the pH at 8, in anaerobic digestate of piggery effluent has
been shown to significantly increase microalgae growth and pro-
ductivity [48]. The CO2 addition abated the decrease in productivity
observed at extreme concentrations of ammonia. The low mass transfer
efficiency of CO2 from gaseous to liquid phase is one of the major
limiting factors in microalgae cultivation [128]. The direct injection of
gases into microalgae culture, which always accompanies the release of
CO2 to the atmosphere, may not be as effective if smart designs and
methods to either increase the diffusivity, increase retention time and/
or reduce the gas bubble size, are not employed.
Dissolved inorganic carbon (DIC) exists as either CO2, HCO3− or
CO32− and the proportions of each species depend on pH and tem-
perature. Microalgae preferentially take up CO2 through passive diffu-
sion, over HCO3− which relies on active transport. However, at high pH
most DIC in wastewater is in the form of HCO3− and CO32−, with in-
significant available CO2 [129]. The addition of CO2 results in de-
creasing pH and shifts the DIC equilibrium, thereby increasing the
availability of CO2. In a study on the effect of the addition of CO2 along
a pH gradient on wastewater microalgal photo-physiology [119], the
decrease of pH from 8 to 6.5, with the addition of CO2 resulted in a
significant increase in Dissolved Inorganic Carbon and consequently a
significant increase in biomass. The highest biomass yield was achieved
at the highest DIC/lowest pH combination [119]. However, the in-
creased microalgal biomass did not have any significant effect on am-
monia volatilization. This was described to likely be an artifact of the
pond design, resulting in very high ammonia volatilization. This
method, in addition to an adequate bioreactor design, could be used for
the treatment of anaerobic digestate effluent lending itself also as a
means to reduce ammonia volatilization.
In anaerobic digestions plants, CO2 for the cultivation of microalgae
can be sourced in-house. However, the additional cost of capture and
transportation/transmission must be considered. Depending on how
biogas is utilized, there are different routes to capture CO2. Biogas
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Algal Research 47 (2020) 101841
mainly consists of methane (CH4 ~ 65 vol%) and carbon dioxide (CO2
~ 35 vol%), an upgrading process is normally needed to remove CO2
and other unwanted impurities before it can be used as vehicle fuel. The
CO2 removed from the raw biogas can be captured and stored, leaving
clean biomethane. Capturing CO2 from biogas upgrading can be cate-
gorized as pre-combustion capture [130]. When raw biogas is directly
used to produce power and heat through combined heat and power
(CHP) generators or burning in a combustor, the CO2 is captured from
the exhaust gas. Capturing CO2 this way is categorized as post-com-
bustion capture. Pre-combustion capture yields higher CO2 concentra-
tions and purity due to the high CO2 content of raw biogas. On the other
hand, using biogas as fuel results in a low CO2 content in the exhaust
gas; therefore, post-combustion capture from exhaust yields much
lower CO2. Microalgae cultures can also be used to capture CO2 directly
from biogas by injecting the biogas into a closed algal cultivation
system e.g. closed glass photobioreactors and photobioreactor bags,
simultaneously upgrading the biogas and using CO2 as carbon source
[85,89,90] (see Table 4 for CO2 removal efficiencies).
3.3.2. Strain selection, acclimation, and diversification
A potential solution to the problem of nutrient/Ammonia toxicity in
the cultivation of microalgae in ADFE is the proper selection, diversi-
fication, and/or acclimation of algal strains. Native species have been
shown to perform better than other species in the commercial-scale
cultivation of microalgae in wastewater [131,132]. Acclimation, in
accordance with the local environment, can facilitate the growth of
native species and even physiological acclimation of commercial cells
in wastewater before their utilization has been shown to improve nu-
trient removal efficiency [133]. The exact mechanisms through which
microalgae adapt and acclimatize to toxic nutrient conditions in was-
tewater are unclear. However, acclimation to wastewater tolerance has
been shown to correlate with higher accumulation of carotenoid pig-
ments and increased ascorbate peroxidase activity [134].
High-diversity native microalgal systems can also result in more
robust operation and higher productivity. Compared to monocultures,
microalgal consortia of higher diversity are considered to be more
stable (Lau et al. 1996) and less susceptible to invasion [135]. The di-
versification of microalgae in cultivation systems can have a positive
effect on the stability of the ecosystem, and the use of consortia with
species possessing different metabolic abilities or strains with different
light absorption spectrum enhances nutrient retention [136–138] as
well as overall remediation capacity [139]. Also, mixed culture systems
are cheaper and easier to operate and maintain [140].
Recently, Ayre et al. [48] successfully isolated microalgae from
several freshwater and wastewater samples, combined and further ac-
climatized them resulting in a mixed culture containing at least three
microalgae species capable of growing on Anaerobic digestate effluent
of Piggery Effluent with Ammonia Nitrogen content up to 1600 mg L−1.
They were able to achieve biomass productivity of 315 mg m−2 d−1 in
outdoor raceway pond with the addition of CO2, keeping pH at 8
without optimizations or significant pre-treatment of the digestate. It is
to be noted that the study was mostly directed towards the acclimation
of the microalgal consortium in undiluted ADPE, and no real attempt
was made to optimize any other growth parameters. Their results de-
monstrated that microalgae consortium can be cultivated in undiluted
ADPE to avoid using fresh water for dilution but the very high NH3-N
content (1600 mg L−1) led to low productivity.
3.3.3. Optimal and innovative pond and bioreactor designs
As previously stated, the most significant limitation to the cultiva-
tion and growth of algae is light quality and quantity, and this limita-
tion is more pronounced when dealing with turbid substrates like
anaerobic digestates. Pond and bioreactor designs that improve the
distribution and utilization of light are a definite ‘yes’ for the cultivation
of algae using Anaerobic digestates. In the next sections, we discuss the
available cultivation systems used for mass algal production with an
D. Chuka-ogwude, et al.
emphasis on wastewater treatment.
4. Microalgal cultivation systems
Algal cultivation systems can be broadly classified into open, closed,
hybrid, and biofilm systems. In open ponds, the algal biomass is ex-
posed to the environment. Although open ponds are less expensive to
build and operate, they are limited by the inability to adequately con-
trol growth conditions such as irradiance levels, temperature, and
contamination. Open ponds include paddlewheel driven raceway
ponds, inclined thin layer ponds, circular ponds, and lagoons ponds.
Closed cultivation systems offer better control over growth conditions
and consequently allow for higher productivities in comparison to open
ponds. However, closed cultivation systems are significantly more ex-
pensive than open systems to set up and operate. Closed cultivation
systems include tubular photobioreactors, flat panel photobioreactors,
helical tubular photobioreactors, and plate photobioreactors (vertical
and horizontal). Other cultivation systems that do not immediately fit
into the categorization stated above are biofilm (solid) and hybrid
cultivation systems. The following sections discuss applications of some
of the cultivation systems mentioned above for the treatments of
anaerobic digestate effluent.
4.1. Open pond cultivation systems
Owing to less capital costs and simplicity in construction, open
ponds are the most commonly used cultivation systems for mass algae
cultivation [141]. Open cultivation systems include paddlewheel driven
raceway ponds, thin layer ponds, circular ponds, and lagoons.
4.1.1. Raceway ponds
General raceway pond configurations consist of a closed circular
loop typically with depth about 0.25–0.30 m (Fig. 1). Lower depths are
preferred to improve light penetration, but depth cannot be much <
0.30 m for large scale ponds [141]. Typically, the length of the strait of
the loop should be significantly larger than the width of the raceway.
This is important because if this ratio is too low flow disturbances at the
end of the bends begin to affect the flow in the straight channel leading
to increased power consumption and dead zones, ultimately leading to
inadequate mixing. A high surface-to-volume ratio of the raceways is
intended to provide a large area for absorption of the sunlight required
by microalgae to grow [142]. Flow requirements in the pond should be
such that flow is not laminar but turbulent to prevent algal cells from
settling at the bottom of the pond. Conditions should be optimized such
that turbulence thresholds are not exceeded, resulting in turbulence
stress and death of cells in the medium [142]. Raceway ponds are the
Fig. 1. Left – Open raceway pond; source: [148]. Right- High rate algal pond; source: [149].
8
Algal Research 47 (2020) 101841
most used open cultivation systems but are limited by low productivity
and high risk of contamination by other algae, bacteria, and protozoa
which can diminish overall biomass productivity and even outcompete
the desired microalgae [141].
Raceway ponds are frequently used in the treatment of wastewater
effluents and have been used in the treatment of anaerobic digestate
effluent, both diluted [102] and undiluted [48,103], with various levels
of biomass productivity and nutrient removal rates. This and further
examples are listed in Table 4.
High rate algal ponds are shallow raceway ponds (Fig. 1) that were
developed for wastewater treatment by Oswald and his colleagues in
the 1950s [143]. The term ‘high- rate pond’ was first used by Oswald to
describe raceway ponds that differ from other pond systems in that they
aimed to maximize their algal biomass concentration to increase their
wastewater treatment efficiency. The depth of the ponds is dependent
on the turbidity/clarity of the wastewater being treated, typically be-
tween 0.2 and 0.6 m. Paddlewheel mixing (0.15–0.3 m/s) causes tur-
bulent eddy currents that provide horizontal and some vertical mixing
in the pond, required for the intermittent exposure of algae to sunlight
[144]. High rate algal ponds are frequently coupled with Anaerobic
ponds and the substrate used in high rate algal ponds is the supernatant
from anaerobic or facultative ponds. Though they are not generally
used for the direct treatment of anaerobic digestate effluents, they are
used extensively for the treatment of wastewater [144–146] and their
closeness to the subject of anaerobic digestion warrants mention.
High rate algal ponds are considered low-cost due to less cost of
operation, shorter hydraulic retention time, and cheaper construction
costs in comparison with other wastewater treatment systems such as
activated sludge systems [147]. High rate algal ponds retain the ad-
vantages of conventional ponds (anaerobic, facultative) owing to sim-
plicity and economy but overcome many of their disadvantages (poor
and inconsistent effluent quality, limited nutrient and pathogen re-
moval) and have the added benefit of recovering nutrients into har-
vestable algal biomass for beneficial use as fertilizer, feed or biofuel
[147].
4.1.2. Inclined thin layer ponds
Inclined thin layer ponds are open ponds inclined at an angle
(Fig. 2). In this system, algae culture flows down the inclined surface in
a thin layer. The algae culture is collected at the bottom end of the pond
and recirculated to the top of the incline by a pump to repeat the flow
[141]. Inclined thin layer ponds were first developed in the Czech Re-
public [150] where the system was operated at culture depth of
4–6 mm, and flow rate of 8 cm.s−1 with continuous circulated down a
3% inclined glass surface during the day. At night the culture suspen-
sion was kept in an aerated tank. This operation was found to reduce
D. Chuka-ogwude, et al.
Fig. 2. Left – Open Thin-layer inclined cascade photobioreactor. Source: [154]. Right – Thin-layer inclined pond; source: [41]
the overall cost of pumping and reduce the need for cooling the culture
at night. The first thin layer inclined pond systems were fitted with
baffles, which resulted in intensive mixing, limiting algal sedimenta-
tion, and increasing the frequency of exposure of the cells to light and
dark periods [150]. However, the baffles caused the disadvantage of
about two-fold higher investment costs compared with the regular ra-
ceway ponds, high energy consumption for the operation of the pumps,
labor-intensive and time-consuming cleaning process for the inclined
surface. These disadvantages were reduced in subsequent models by
reduced surface inclination and removal of the baffles [151]. The
system was operated at a 6 mm thick layer and was able to reach a very
high algal density at harvest [152].
The advantages of thin layer inclined ponds are as a result of the
shorter light path resulting in lower light attenuation, due to the thin
layer of culture, high turbulence resulting in better mixing, and better
utilization of flashing light (light/dark periods) effect [151–153]. The
advantages associated with thin layer inclined ponds have been ade-
quately substantiated with reports of cell densities and productivities of
4.3 g algal DW L−1 d−1, net areal productivities of 38.2 DW L−1 d−1
with peaks of 50 DW L−1 d−1for the cultivation of Chlorella and Sce-
nedesmus freshwater strains in the Czech Republic and Greece
[152,153].
The advantages (thin culture layers and higher turbulent flow rates)
of inclined thin layer ponds are especially well suited for the case of
anaerobic digestate effluents which have high turbidity resulting in
higher light attenuation. In view of the importance of light diffusion,
Raeisossadati et al. [41] investigated the use of a customized inclined
thin layer pond for treating anaerobic digestate from piggery effluent
under the outdoor climatic conditions of Perth, Western Australia. The
inclined pond was operated at a depth of 5 mm which allowed for
improved light diffusion and better light distribution. The lipid content
of the biomass harvested from the inclined ponds was above 33%, in-
dicating the possible application of the biomass for biodiesel produc-
tion. The inclined thin layer pond had better volumetric productivity in
comparison to the raceway pond (Table 4). However, the raceway pond
had better overall areal productivity. The disparity between the volu-
metric and areal productivities was partly because the inclined pond
had an operational volume of 350 L in comparison with the raceway
pond with an operational volume of 1500 L for the same areal footprint
in additional to other optimization issues. In Raeisossadati et al. [41]
study, the advantage offered by the thin layer inclined pond in terms of
improved light absorption per cell was insufficient to account for a
smaller operational volume per unit area. Volumetric productivity for
the thin layer inclined pond will need to be much higher to favorably
compete with the open raceway pond in terms of areal productivity. In
other words, the cells should be able to absorb all the incident light (no
9
Algal Research 47 (2020) 101841
light loss) and maximally utilize all the absorbed light (no light in-
hibition) to achieve maximum productivity. This calls for optimization
of the thin layer open pond depth to achieve higher standing biomass
concentration yield resulting in higher areal productivity. Further stu-
dies on optimizing the inclined pond with various depths were sug-
gested and some opinions for such optimizations are discussed in the
following sections.
Optimizations of the depth of inclined thin layer ponds will provide
insight on the limits to light diffusivity and attenuation, especially in
regard to turbid substrates like undiluted anaerobic digestate effluents.
Though the higher turbulent flow rates of inclined thin layer ponds
provide better mixing capabilities, there might be a need for even more
systematic mixing for better light utilization given the nature of anae-
robic digestate effluents.
4.1.3. Other open cultivation systems
Other open cultivation systems used in the treatment of wastewaters
are Shallow lagoons and ponds, and Mixed ponds [141]. Shallow algae
lagoons, ponds, and ditches are the oldest form of wastewater treatment
methods and have been used for thousands of years. Mixing in lagoons
and ponds is done by wind and convection and by careful management
of the flow of fluids through the ponds. Areal productivity in shallow
lagoons and ponds is characteristically low [141]. Mixed ponds are
typically about 50–80 cm deep and the simplest kind of mixing is with
aeration from the bottom of the pond. However, mixing is mostly un-
even and consequently, productivities are low [141].
4.2. Closed photobioreactors
Closed cultivation systems for cultivating microalge are generally
made up of transparent plastic or glass [155]. Closed photobioreactors
have lent themselves to several innovative designs but are majorly di-
vided into three types of designs: flat plate, tubular (Fig. 3) and bag
photobioreactors [155]. The advantages of the closed photobioreactors
include the ability to control the culture conditions (e.g., temperature,
pH, irradiance), manage contamination more effectively and reduced
water loss due to evaporation which is prevalent in open systems; de-
pendent on climate conditions viz.: solar radiation and wind velocity
[156]. Mixing in closed photobioreactors is achieved by recirculation
using airlifts systems or external pumps [155,157]. Closed photo-
bioreactor systems have been shown to produce high algal cell densities
of up to 20 gL−1 allowing for a significant reduction in harvesting cost
and capital cost of the photobioreactors [155,158]. In addition to dis-
advantages of high capital and operational cost associated with closed
photobioreactors stated earlier, there is also the problem of biomass
inhibition due to high concentrations of dissolved oxygen (DO).
D. Chuka-ogwude, et al.
Fig. 3. Biocoil photobioreactor; Source: Algae R&D Center, Murdoch
University.
Difficulty in dealing with DO has been shown to cause culture crash and
also has been fingered as a major factor in limiting the scaling up of
closed systems [159]. The inhibitory effect of dissolved oxygen is ma-
jorly due to the competitive inhibition of photosynthesis by dioxygen
(O2), as O2 competes with CO2 for the active site of Ribulose-1,5-bi-
sphosphate carboxylase oxygenase (RuBisCo) [160]. At higher DO
concentrations, the result is reduced biomass productivity due to the
photosynthetically wasteful process of photorespiration [161]. Also
associated with high DO is the prevalence of reactive oxygen species
(ROS) that may cause severe inhibition and damage the photosynthetic
apparatus, cellular membranes, DNA, and other cellular components of
microalgal cells [159]. Although high DO concentrations is also an issue
with open pond cultivation systems, it is less prominent and can be
relatively easily ameliorated by deoxygenation systems involving some
form of circulation method [162].
Currently closed photobioreactors are only used commercially for
the production of high valued products due to the high capital and
operational cost [157]. Pilot-scale applications of tubular airlift pho-
tobioreactor systems in the treatment of wastewater have been de-
monstrated but, in addition to the high cost of manufacturing, it is
prone to severe biofouling [163]. Work has also been done on the ap-
plication of closed photobioreactors for the treatment of diluted anae-
robic digestate of swine slurry [164] and anaerobic digestate of swine
slurry [48,103] with various biomass productivities and nutrient re-
moval rates. However, the costs associated with them outweigh any
apparent advantages.
4.3. Hybrid cultivation systems
Hybrid cultivation systems combine two or more bioreactors into a
single process, usually in multi phases presenting a synergistic effect
exploiting the advantages of both cultivation systems while minimizing
inherent setbacks of the daughter systems, such as high production cost
associated with photobioreactors and contamination in raceway ponds
[165]. Applications of hybrid systems include the use of closed photo-
bioreactor systems in combination with raceway ponds for the multi-
stage cultivation of algae. Examples include combining biomass pro-
duction in air lift-driven closed bioreactors with a separate high-lipid
induction phase in nutrient deplete raceway ponds [165–167].
The advantage of hybrid systems is that each part of the system can
exploit its advantages to maximal levels and they are especially suited
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Algal Research 47 (2020) 101841
for processes that can be disjointed into multiple stages as exemplified
above. The disadvantages include high capital and operational costs,
especially if high valued products are not being produced. Currently,
there is no literature on the use of hybrid photobioreactor systems in
the treatment of anaerobic digestate effluent, but the intuition of the
system is straightforward and can be adopted and adapted if the eco-
nomics are right.
4.4. Biofilm cultivation systems
Microalgal biofilm culture systems are an alternative to suspension-
based cultivation systems found in both open and closed algal culture
systems. Microalgal biofilm systems have the distinct benefit of redu-
cing the cost associated with harvesting algal cells [168–171]. In mi-
croalgal biofilm systems, the algae cells are attached to a material
surface, keeping them in place while nutrients run over the surface.
Cells are harvested after cultivation by scraping them off the surface of
the material [172,173]. The harvested cells have a high solid content
which has been demonstrated to be as high as 10–20% obtained in a
rotating algal biofilm (RAB) cultivation system [174]. This is similar to
what is obtainable in post-centrifuged algal biomass from suspension-
based cultivation systems. Microalgal biofilm systems also have the
advantage of minimizing light limitation and enhancing of CO2 mass
transfer. Solid retention time of cells without wash-out is also increased
because of the separation of the cells and the liquid medium [170].
Biofilm cultivation systems can also be selective in regard to the
type and species of cultivated algae. This is because the propensity of
the microalgae strain to attach to the surface of the attachment material
is a critical factor. The tendency of microalgae cells to attach to the
surface of any material depends on the surface properties of both the
microalgae (this varies between and within species) and the substrate
[170]. Compatible surface hydrophobicity of the solid supports and the
cells is an essential parameter for defining the mechanism of cellular
adhesion to the solid surfaces [175]. Generally, microalgae cells have
negatively charged surfaces that help repel other negatively charged
cells and thus prevent unnecessary flocculation [176]. The strength of
the negative charge also determines the hydrophobicity of the cell
membrane, and cells that are more hydrophobic tend to form biofilms
more easily [177].
Over time, several microalgal biofilm systems have been developed
depending on the desired application, with different geometry, at-
tachment material, and orientation. They can be classified into per-
fused, submerged, horizontal, vertical, and rotating systems [178,179].
Inclined microalgal biofilm reactors, belonging to the perfused systems,
have been established as being the most efficient as limitations owing to
less contact time observed in vertical reactors and inefficient light
utilization in horizontal reactors can be minimized by using an inclined
support system [170]. Also, submerged systems like Algal Turf Scrubber
(ATS™) (Fig. 4), phototrophic biofilm incubator, biofilm flow cell, ro-
tating microalgal biofilm reactor (RABR) have been successfully de-
veloped at large scales for wastewater treatment [104,169,172].
There is evidence of high biomass areal productivities using mi-
croalgal biofilm systems [180], and areal productivities have been re-
corded to be as high as 25–31 g m−2d−1 [104,172]. However, the
systems face challenges of high evaporation losses and high operating
costs. Though biofilm cultivation systems might be uniquely suited for
use with turbid substrates (owing to a very thin fluid layer of the
substrate), the available literature reports on microalgal biofilms sys-
tems are limited to municipal wastewater with only few studies on
animal manure and anaerobic digestate [104,180] (Table 4).
4.5. Optimizations in cultivation systems design
Since dilution, to reduce turbidity, is deemed inefficient then in-
novations in bioreactors must focus on smarter ways to deal with light
attenuation and light utilization. Optimizations in bioreactor design can
D. Chuka-ogwude, et al.
Fig. 4. Biofilm Algal Turf Scrubber raceway (ATS™); Source: [104].
also help to alleviate problems arising from the low mass transfer ef-
ficiency of CO2 from gaseous to liquid phase, increase residence time,
retention, and diffusivity of CO2.
In regard to light utilization, two polar cases must be considered,
and a proper balance struck between them. These cases are photo-
limitation and photoinhibition. As the terms imply, photolimitation
occurs when the light available is not sufficient (low irradiance) to
allow for maximal algal growth while photoinhibition, which can lead
to photodamage, occurs when the light available is in excess (excessive
irradiance) of the saturation point for algal growth. As stated pre-
viously, photosynthesis is seen to correlate with an increase in light
irradiance until maximum algal growth is achieved at the light sa-
turation point, so light distribution should be such that it is between
these limits. In cultivation systems, the effect of zones of photolimita-
tion (dark zones) increases collinearly with cell biomass concentration
and productivity decreases until zero in those zones [181]. In turbid
substrates like digestates, high light attenuation and decreased pro-
ductivity due to dark zones is even more pronounced leading to more
algae cells being subjected to photolimitation and photoinhibition
further increasing the need for better light distribution systems in ponds
and bioreactors. Light distribution systems are mainly divided into two:
temporal and spatial light dilution systems [182].
Temporal dilution is based on high turbulence, moving the algae
cells rapidly between the light and dark zones of the culture vessel. This
is also termed the ‘flashing light effect.’ This leads to a dilution of the
photosynthetic photon flux density (PPFD) over time [182]. It has been
known for years now that the efficiency of light utilization by micro-
algae can be significantly increased by exposing the cells to alternating
periods of light and dark [183]. However, it has also been established
that random turbulence is insufficient to take full advantage of the
flashing light effect to any significant degree [184] and utilization of
the flashing light effect requires a nonrandom mixing pattern in which
11
Algal Research 47 (2020) 101841
cells are exposed to regular cycles of light and dark [185]. Vortex
generating devices like airfoils, delta wings, baffles, cylinders, etc. can
be installed in photobioreactors. Foils similar to airplane wings to
create systematic mixing in a raceway pond increased photosynthetic
efficiencies in an experimental culture of P. tricornutum 2.2–2.4 folds
[183]. Huang et al. [186] simulated the hydrodynamic characteristics
of wing baffles similar to those used by Laws et al. [183] in a raceway
pond to achieve biomass increase of 30.1%. The raceway with installed
wing baffles produced 127% increase in velocity in the direction of light
attenuation (vertical velocity). However, these wings increased flow
resistance, thus increasing energy consumption. Similar design with
wing baffles in raceway ponds resulted in significant increases in bio-
mass and vertical velocity [187,188]. Addition of baffles in inclined
thin layer ponds have also been investigated [151] indicating increased
productivity but at the cost of increased power and labor. Depth opti-
mization for the channel flow in inclined thin layer ponds potentially
could improve productivity significantly. In a regular raceway pond,
there is sufficient culture depth to absorb all the incident photons into
the system, (the actual usage of the photons by the cells is another
issue) leading to a spatial productivity (condition of possible photo-
inhibition at the surface from high irradiance, a region with optimum
productivity, and photolimitation at the bottom of the pond where no
light is available). The incident photons received/reaching the surface
area of the inclined thin layer pond will not all be absorbed by the
microalgae cells and this is even more obvious in a thin layer pond.
Being that the layer of microalgae flow is very thin, a lot of the photons
reaching the surface of the pond will be lost as heat and by reflectance
from the bottom of the pond. Only a proportion will be absorbed by the
algae (this is a function of the light path, the mass absorption coefficient
of the algae cells and the culture biomass concentration). In climates of
high solar irradiance there might be significant photoinhibition on the
surface of the incline. Increasing the depth of the flow should allow for
D. Chuka-ogwude, et al.
Fig. 5. Microalgal culture to treat ADFE flow chart.
some temporal diffusion of the light allowing for more penetration to
the deeper depths. Moheimani and Borowitzka [189] have demon-
strated that pond depth in a regular raceway pond was a significant
factor in increasing the productivity of microalgae due to the reduction
of dark zones (and photolimitation) at the bottom of the ponds. The
same reasoning can be applied to inclined thin layer ponds. Temporal
light diffusion/flashing light systems are effective and more suited to
open pond cultivation systems and invariably, may be more suited for
application in the optimization of cultivation systems used to treat
anaerobic digestates.
Spatial diffusion systems collect light/irradiance and distribute it
over larger surface areas. The idea is to effectively collect irradiance
and deliver to microalgal cultures at saturation light intensities and
thus, effectively reducing effects of photoinhibition [182]. These sys-
tems can also be used to direct light to the inside and depths of culture
vessels, thereby helping to alleviate the problem of photolimitation.
Examples of spatial distribution systems include Luminescent Solar
Concentrators (LSCs), optical fibers and translucent cones. The earliest
application of spatial diffusion was with the use of glass and plastic
cones to distribute light over larger surfaces/depths of a small scale
algal bioreactors cultivating Chlorella sp. and saw an increase of 2 folds
for biomass yields [190,191]. Translucent Perspex cones have also been
used to spread light into a 1-m deep pond reducing photolimitation and
increasing productivity by 28% [192]. Takano et al. [193] used light
diffuser optical fiber (LDOF) bundles to spread light to the middle of a
bubble column photobioreactor and were able to increase biomass
productivity 4.2 folds. Using LSCs for microalgae cultivation systems
have been reported with varying levels of improved productivities
[194–197]. Ogbonna et al. [198] used Fresnel lenses to collect solar
light (also filtering off most of the ultraviolet and infrared wavelengths)
and distributed the solar light using optical fibers into indoor photo-
bioreactors. Some of these systems (e.g., optical fibers) may be better
suited for closed photobioreactors than they are for open ponds while
some (e.g., translucent cones) may be better suited for open ponds. The
cost, however, must be carefully considered. Generally, spatial diffusion
systems are considered more expensive than temporal diffusion systems
and are not frequently used in open cultivation systems. However, there
are arguments to the contrary [199].
Cultivation of algae in Anaerobic digestate will almost certainly be
12
Algal Research 47 (2020) 101841
done using outdoor, open cultivation systems since low cost and sim-
plicity are strongly desired. Therefore, light utilization optimization
systems should lean towards systems that are easily and cost-effectively
applicable to open systems.
An advantage that temporal light diffusion methods have over
spatial diffusion methods is that it, by virtue of its nature and config-
uration, increases mass transfer. There is evidence of the increase in
bubble dispersion and volumetric mass transfer in both raceway ponds
[200,201] and closed photobioreactors [202] due to vortices and ver-
tical mixing. Cheng et al. [201] investigated the effect of permutated
conic baffles generating both vertical and horizontal vortex flow and
reported that vertical shear produced by vertical vortices decreased
bubble diameter and generation time of CO2 injected into the medium,
while horizontal shear increased residence time. There is also report
that vertical mixing, and vertical vortices increase CO2 residence time
and increase bubble generation time in optimized flow fields in raceway
pond. The decreased generation time and increased residence time of
the bubbles promoted microalgae biomass yield by 29% [203]. The
geometry of the CO2 diffusers used to inject CO2 should also be con-
sidered carefully.
Smart application of the above knowledge could allow for a sig-
nificant increase in productivity in the use of anaerobic digestate ef-
fluent as a growth medium for microalgae given the challenges and
limitations of said medium.
5. Economic advantages of microalgal ADFE treatment
The benefits of anaerobic digestion for the treatment of organic
waste cannot be denied but the economics of running anaerobic di-
gestion plants, especially for source segregated food waste, is not ex-
actly attractive, even if it is to be incentivized [20]. In addition to better
process control for anaerobic digestion processes, there is the need for
the re-use of wastes that come from the process (e.g., digestate) for
further product extraction. Anaerobic digestates hold a lot of nutrients
that can be valorized and potentially improve the economics of anae-
robic digestion. For every ton (1000 kg) of feedstock entering an
anaerobic digestion plant, 900 to 950 kg of digestate is produced [4].
Fig. 5 shows potential paths for the utilization of biomass gotten from
the cultivation of microalgae using ADFE.
D. Chuka-ogwude, et al.
Algae biomass gotten from cultivation on ADFE can be converted
into a variety of products. Lipids from the biomass can be converted
into biodiesel [204,205], biomass can also be used as animal feed, or
biofertilizer [97,206], residues from microalgae cultivation can be used
for bioethanol and biobutanol fermentation [207]. The algal biomass
from microalgae cultivation can also be used as feedstock for anaerobic
digestion (Table 2). The water from the treated waste can be used for
other operational and production processes where non-portable water
is required [208]. It has also been shown that the water gotten from the
algal cultivation in digestates can be recycled and used for algal culti-
vation satisfactorily [38]. These all represent potential additional rev-
enue streams and cost cuts for operators of anaerobic digestion plants.
Further, the microalgae debris after lipid extraction can be recycled for
digestion or co-digestion in anaerobic digestion, and is a promising way
to enhance methane production [92,205,209,210]. This can potentially
result in a closed loop for the treatment of food waste. For larger in-
dustrial waste plants of raw biogas capacity ranging between 1000 and
2000 m3 h−1, the costs of biogas upgrading range between $0.09 and
$0.18 per m3 of biomethane produced. This means that for a 30,000
ton/year plant, producing a maximum of 7.8 million m3 of biomethane
per year, upgrading would add between $700,000 and $1,400,000 in
costs [4]. Microalgae cultivation can be utilized for upgrading bio-
methane produced from anaerobic digestion plants while simulta-
neously producing algae biomass [85,90,99] resulting in significant
savings in the process.
Various economic assessments have been made for treatment and
valorization of anaerobic digestates using microalgae and have some-
what come to similar conclusions. A techno-economic analysis made on
the cultivation of microalgae on abattoir waste anaerobic digestate ef-
fluent shows that the approach can be economically feasible if done
right. The significant parameters to consider in the large scale culti-
vation of microalgae are daily algae production (productivity), pond
area, nutrient-depleted water for recycle, total capital expenses
(CAPEX), total operational expenses (OPEX) and algae production cost
[208]. Sensitivity analysis showed that microalgae productivity (spe-
cifically areal productivity) is the most influential parameter on the
economics as it has a direct impact on cultivation area capital cost, cost
of water and OPEX [208]. Techno-economic analysis done of the cul-
tivation of microalgae on anaerobic digestate piggery effluent (ADPE)
also shows that the most critical parameter is areal productivity and
also that open pond systems are more economical when compared to
closed systems like Biocoils [211]. These techno-economic analysis al-
ludes to the fact that selection of tolerant, high-performance strains,
and cultivation process optimization are integral to making microalgal
cultivation on anaerobic digestate effluent economically feasible.
6. Conclusions
Anaerobic digestion is a reliable technology for recycling bioenergy
from food waste. However, it leaves a waste product in the form of
anaerobic digestate effluent with a significant amount of nutrients, that
itself is difficult to dispose of effectively. The use of algae to reduce the
nutrient load of ADFE is a viable option because of the many oppor-
tunities that algae propagation affords and the cost cuts using anaerobic
digestate effluent as a nutrient source for algae allows. Also, the va-
lorization of waste (anaerobic digestate effluent) from the anaerobic
digestion of food waste will improve the economics of anaerobic di-
gestion processes. The use of digestate as a nutrient source for the
cultivation of algae has its challenges due to high turbidity and toxic
nutrient concentrations. The paths to improvement of the treatment
and valorization of ADFE with microalgae lay in the selection of mi-
croalgal strains able to tolerate the toxic nutrient concentrations of
ADFE and smart photobioreactor/pond designs to maximize light uti-
lization and photosynthetic efficiencies of the algae considering the
turbidity of ADFE.
Recent attempts to acclimatize and cultivate microalgae in very
13
Algal Research 47 (2020) 101841
high concentrations of ADPE [48] has greatly emphasized the potential
of that approach, setting the pace for further bioprospecting and ac-
climation studies and application to other digestates (e.g., ADFE). Also,
innovative cultivation ponds like the inclined thin layer pond are un-
iquely suited for the use of ADFE owing to its ability to support high
concentrations of algal biomass. The advantages of the inclined thin
layer pond, as stated previously, lies in its thin layer of cultivation
enabling a much shorter light path and consequently reduced light at-
tenuation. However, optimizations in terms of temporal light diffusion,
operational depth, and operational inclination are to be made and have
also been suggested by its innovators [151–153,212]. Thus far no lit-
erature is available on the use of Inclined Thin Layer ponds in the
cultivation of algae using ADFE, or on the optimization of the depth,
inclination and mixing speed of the thin layer inclined pond.
Statement of informed consent, human/animal rights
No conflicts, informed consent, human/animal rights applicable.
Authors' declaration
All authors agree to authorship and submission of the manuscript
for peer review.
CRediT authorship contribution statement
David Chuka-ogwude:Conceptualization, Investigation,
Methodology, Writing - original draft, Writing - review &
editing.James Ogbonna:Funding acquisition, Resources,
Supervision, Validation, Writing - review & editing.Navid R.
Moheimani:Conceptualization, Funding acquisition, Investigation,
Methodology, Resources, Supervision, Writing - review & editing.
Declaration of competing interest
The authors report no relationships that could be construed as a
conflict of interest.
Acknowledgements
This research was financially supported by Murdoch University.
This research received no other specific grant from any funding agency
in the public, commercial or not-profit-sector.
References
[1] FAO, Global Food Losses and Food Waste – Extent, Causes and Prevention, Rome
(2011).
[2] K. Paritosh, S.K. Kushwaha, M. Yadav, N. Pareek, A. Chawade, V. Vivekanand,
Food waste to energy: an overview of sustainable approaches for food waste
management and nutrient recycling, Biomed. Res. Int. 2017 (2017).
[3] FAO, Save Food for a Better Climate, (2017).
[4] S. Jain, D. Newman, R. Cepeda-Márquez, K. Zeller, Global Food Waste
Management: An Implamentation Guide for Cities. Full Report, (2018).
[5] S. Kaza, L. Yao, P. Bhada-Tata, F. Van Woerden, What a Waste 2.0, a Global
Snapshot of Solid Waste Management to 2050, (2018).
[6] C. Zhang, H. Su, J. Baeyens, T. Tan, Reviewing the anaerobic digestion of food
waste for biogas production, Renew. Sust. Energ. Rev. 38 (2014) 383–392.
[7] J. Huang, P.N. Nkrumah, D.O. Anim, E-waste disposal effects on the aquatic en-
vironment: Accra, Ghana, Rev. Environ. Contam. Toxicol. 229 (April) (2014)
19–34.
[8] S.A. Opatokun, T. Kan, A. Al Shoaibi, C. Srinivasakannan, V. Strezov,
Characterization of food waste and its digestate as feedstock for thermochemical
processing, Energy and Fuels 30 (3) (2016) 1589–1597.
[9] C.J. Banks, M. Chesshire, S. Heaven, R. Arnold, Anaerobic digestion of source-
segregated domestic food waste: performance assessment by mass and energy
balance, Bioresour. Technol. 102 (2) (2011) 612–620.
[10] J.J. Mayers, A. Ekman, E. Albers, K.J. Flynn, Nutrients from anaerobic digestion e
ffl uents for cultivation of the microalga Nannochloropsis sp. — impact on growth,
biochemical composition and the potential for cost and environmental impact
savings, Algal Res. 26 (August) (2017) 275–286.
D. Chuka-ogwude, et al.
[11] J.P. Sheets, L. Yang, X. Ge, Z. Wang, Y. Li, Beyond land application: emerging
technologies for the treatment and reuse of anaerobically digested agricultural and
food waste, Waste Manag. 44 (2015) 94–115.
[12] M.S. Romero-Güiza, J. Vila, J. Mata-Alvarez, J.M. Chimenos, S. Astals, The role of
additives on anaerobic digestion: a review, Renew. Sust. Energ. Rev. 58 (2016)
1486–1499.
[13] K. Moriarty, Feasibility study of anaerobic digestion of food waste in St. Bernard,
Louisiana, Natl. Renew. Energy Lab. (January) (2013).
[14] B. Schink, Energetics of syntrophic cooperation in methanogenic degradation,
Microbiol. Mol. Biol. Rev. 61 (1997) 262–280.
[15] M.E. Griffin, K.D. McMahon, R.I. Mackie, L. Raskin, Methanogenic population
dynamics during start-up of anaerobic digesters treating municipal solid waste and
biosolids, Biotechnol. Bioeng. 57 (1998) 342–355.
[16] D. Karakashev, D.J. Batstone, I. Angelidaki, Influence of environmental conditions
on Methanogenic compositions in anaerobic biogas reactors influence of en-
vironmental conditions on Methanogenic compositions in anaerobic biogas re-
actors, Appl. Environ. Microbiol. 71 (1) (2005) 331–338.
[17] F. Xu, Y. Li, X. Ge, L. Yang, Y. Li, Anaerobic digestion of food waste – challenges
and opportunities, Bioresour. Technol. 247 (September) (2018) 1047–1058.
[18] Food Waste Reduction Alliance, Analysis of U.S. Food Waste Among
Manufacturers, Retailers, and Restaurants, (2016).
[19] N. Curry, P. Pillay, Biogas prediction and design of a food waste to energy system
for the urban environment, Renew. Energy 41 (2012) 200–209.
[20] M. Franchetti, A. Dellinger, Economic feasibility of a municipal food waste col-
lection and energy generation model, Energy Technol. Policy 1 (1) (2014) 52–58.
[21] M. Dębowski, S. Szwaja, M. Zieliński, M. Kisielewska, E. Stańczyk-Mazanek, The
influence of anaerobic digestion effluents (ADEs) used as the nutrient sources for
chlorella sp. cultivation on fermentative biogas production, Waste and Biomass
Valorization 8 (4) (2017) 1153–1161.
[22] J.M. Owens, D.P. Chynoweth, Biochemical methane potential of municipal solid
waste (Msw) components, Waf. Sci Tech 27 (2) (1993) 1–14.
[23] M.J. Cuetos, X. Gómez, M. Otero, A. Morán, Anaerobic digestion of solid slaugh-
terhouse waste (SHW) at laboratory scale: influence of co-digestion with the or-
ganic fraction of municipal solid waste (OFMSW), Biochem. Eng. J. 40 (1) (2008)
99–106.
[24] D.P. Chynoweth, C.E. Turick, J.M. Owens, D.E. Jerger, M.W. Peck, Biochemical
methane potential of biomass and waste feedstocks, Biomass Bioenergy 5 (1)
(1993) 95–111.
[25] S.J. Grimberg, D. Hilderbrandt, M. Kinnunen, S. Rogers, Anaerobic digestion of
food waste through the operation of a mesophilic two-phase pilot scale digester -
assessment of variable loadings on system performance, Bioresour. Technol. 178
(2015) 226–229.
[26] J.K. Cho, S.C. Park, H.N. Chang, Biochemical methane potential and solid state
anaerobic digestion of Korean food wastes, Bioresour. Technol. 52 (3) (1995)
245–253.
[27] P. Ayala-parra, Y. Liu, J.A. Field, R. Sierra-alvarez, Nutrient recovery and biogas
generation from the anaerobic digestion of waste biomass from algal biofuel
production, Renew. Energy, Vol. 108, No. August (2017) 410–416.
[28] R. Samson, A. LeDuy, Detailed study of anaerobic digestion of Spirulina maxima
algae biomass, Biotechnol. Bioeng. 28 (7) (1986) 1014–1023.
[29] J.H. Mussgnug, V. Klassen, A. Schlüter, O. Kruse, Microalgae as substrates for
fermentative biogas production in a combined biorefinery concept, J. Biotechnol.
150 (1) (2010) 51–56.
[30] S. Buxy, R. Diltz, P. Pullammanappallil, Biogasification of marine algae
Nannochloropsis Oculata, Materials Challenges in Alternative and Renewable
Energy II, John Wiley & Sons, Ltd, 2013, pp. 59–67.
[31] S.K. Prajapati, P. Kumar, A. Malik, V.K. Vijay, Bioconversion of algae to methane
and subsequent utilization of digestate for algae cultivation: a closed loop bioe-
nergy generation process, Bioresour. Technol. 158 (2014) 174–180.
[32] A.F. Torres Franco, S. da Encarnação Araújo, F. Passos, C.A. de Lemos
Chernicharo, C.R. Mota Filho, C. Cunha Figueredo, Treatment of food waste di-
gestate using microalgae-based systems with low-intensity light-emitting diodes,
Water Sci. Technol. (2018) wst2018198.
[33] X. Lei, N. Sugiura, C. Feng, T. Maekawa, Pretreatment of anaerobic digestion ef-
fluent with ammonia stripping and biogas purification, J. Hazard. Mater. 145 (3)
(2007) 391–397.
[34] J. Park, H.F. Jin, B.R. Lim, K.Y. Park, K. Lee, Ammonia removal from anaerobic
digestion effluent of livestock waste using green alga Scenedesmus sp, Bioresour.
Technol. 101 (22) (2010) 8649–8657.
[35] L. Zhang, et al., Cultivation of microalgae using anaerobically digested effluent
from kitchen waste as a nutrient source for biodiesel production, Renew. Energy
115 (2018) 276–287.
[36] W. Peng, A. Pivato, Sustainable management of digestate from the organic fraction
of municipal solid waste and food waste under the concepts of Back to earth al-
ternatives and circular economy, Waste and Biomass Valorization 0 (0) (2017)
1–17.
[37] D.Y. Shin, H.U. Cho, J.C. Utomo, Y.N. Choi, X. Xu, J.M. Park, Biodiesel production
from Scenedesmus bijuga grown in anaerobically digested food wastewater effluent,
Bioresour. Technol. 184 (2015) 215–221.
[38] E.G. Nwoba, B.S. Mickan, N.R. Moheimani, Chlorella sp. growth under batch and
fed-batch conditions with effluent recycling when treating the effluent of food
waste anaerobic digestate, J. Appl. Phycol. 31 (2019) 3545–3556.
[39] Z. Yu, M. Song, H. Pei, F. Han, L. Jiang, Q. Hou, The growth characteristics and
biodiesel production of ten algae strains cultivated in anaerobically digested ef-
fluent from kitchen waste, Algal Res. 24 (27) (2017) 265–275.
[40] J. Cheng, Q. Ye, J. Xu, Z. Yang, J. Zhou, K. Cen, Improving pollutants removal by
14
Algal Research 47 (2020) 101841
microalgae Chlorella PY-ZU1 with 15% CO2 from undiluted anaerobic digestion
effluent of food wastes with ozonation pretreatment, Bioresour. Technol. 216
(2016) 273–279.
[41] M. Raeisossadati, A. Vadiveloo, P.A. Bahri, D. Parlevliet, N.R. Moheimani,
Treating anaerobically digested piggery effluent (ADPE) using microalgae in thin
layer reactor and raceway pond, J. Appl. Phycol. 31 (2019) 2311–2319.
[42] A. Akhiar, Characterization of Liquid Fraction of Digestates after Solid-Liquid
Separation from Anaerobic Co-Digestion Plants, Université Montpellier, 2017.
[43] E. Tampio, T. Salo, J. Rintala, Agronomic characteristics of five different urban
waste digestates, J. Environ. Mangement 169 (2016) 293–302.
[44] S.G. Sommer, S. Husted, The chemical buffer system in raw and digested animal
slurry, J. Agric. Sci. 124 (1995) 45–53.
[45] K. Möller, W. Stinner, A. Deuker, G. Leithold, Effects of different manuring systems
with and without biogas digestion on nitrogen cycle and crop yield in mixed or-
ganic dairy farming systems, Nutr. Cycl. Agroecosystems 82 (2008) 209–232.
[46] K. Möller, T. Müller, Effects of anaerobic digestion on digestate nutrient avail-
ability and crop growth: a review, Eng. Life Sci. 12 (3) (2012) 242–257.
[47] H.A. Abu Hajar, R. Guy Riefler, B.J. Stuart, Anaerobic digestate as a nutrient
medium for the growth of the green microalgae Neochloris oleoabundans, Environ.
Eng. Res 21 (3) (2016) 265–275.
[48] J.M. Ayre, N.R. Moheimani, M.A. Borowitzka, Growth of microalgae on undiluted
anaerobic digestate of piggery effluent with high ammonium concentrations, Algal
Res. 24 (2017) 218–226.
[49] J.N. Galloway, J.D. Aber, J.W. Erisman, S.P. Seitzinger, R.W. Howarth,
E.B. Cowling, The nitrogen cascade, Bioscience 53 (2003) 341–356.
[50] T. Rehl, J. Müller, Life cycle assessment of biogas digestate processing technolo-
gies, Resour. Conserv. Recycl. 56 (1) (2011) 92–104.
[51] R. Nkoa, Agricultural benefits and environmental risks of soil fertilization with
anaerobic digestates: a review, Agron. Sustain. Dev. 34 (2) (2014) 473–492.
[52] Y. Cao, A. Pawłowski, Sewage sludge-to-energy approaches based on anaerobic
digestion and pyrolysis: brief overview and energy efficiency assessment, Renew.
Sust. Energ. Rev. 16 (3) (2012) 1657–1665.
[53] A. Magrí, F. Béline, P. Dabert, Feasibility and interest of the anammox process as
treatment alternative for anaerobic digester supernatants in manure processing -
an overview, J. Environ. Manag. 131 (2013) 170–184.
[54] S. Kizito, S. Wu, S. Mdondo, L. Guo, R. Dong, Evaluation of ammonium adsorption
in biochar- fixed beds for treatment of anaerobically digested swine slurry : ex-
perimental optimization and modeling, Sci. Total Environ. 563–564 (2016)
1095–1104.
[55] S. Kizito, T. Lv, S. Wu, Z. Ajmal, H. Luo, R. Dong, Treatment of anaerobic digested
effluent in biochar-packed vertical flow constructed wetland columns: role of
media and tidal operation, Sci. Total Environ. 592 (2017) 197–205.
[56] E.G. Nwoba, et al., Macroalgae culture to treat anaerobic digestion piggery ef-
fluent (ADPE), Bioresour. Technol. 227 (2017) 15–23.
[57] L. Wang, et al., Anaerobic digested dairy manure as a nutrient supplement for
cultivation of oil-rich green microalgae chlorella sp, Bioresour. Technol. 101 (8)
(2010) 2623–2628.
[58] M. De la Rubia, M. Walker, S. Heaven, C.J. Banks, R. Borja, Preliminary trials of in
situ ammonia stripping from source segregated domestic food waste digestate
using biogas: effect of temperature and flow rate, Bioresour. Technol. 101 (24)
(2010) 9486–9492.
[59] A. Serna-Maza, S. Heaven, C.J. Banks, Ammonia removal in food waste anaerobic
digestion using a side-stream stripping process, Bioresour. Technol. 152 (2014)
307–315.
[60] L. Masse, D.I. Massé, Y. Pellerin, The effect of pH on the separation of manure
nutrients with reverse osmosis membranes, J. Memb. Sci 325 (2) (2008) 914–919.
[61] W. Fuchs, B. Drosg, Assessment of the state of the art of technologies for the
processing of digestate residue from anaerobic digesters, Water Sci. Technol. 67
(9) (2013) 1984–1993.
[62] T. Zhang, K.E. Bowers, J.H. Harrison, S. Chen, Releasing phosphorus from calcium
for Struvite fertilizer production from anaerobically digested dairy effluent, Water
Environ. Res 82 (1) (2010) 34–42.
[63] K. Krishnasamy, J. Nair, B. Bäuml, Hydroponic system for the treatment of
anaerobic liquid, Water Sci. Technol. 65 (7) (2012) 1164–1171.
[64] R. Blowey, J. Wookey, L. Russell, R. Goss, Dried manure solids as a bedding ma-
terial for dairy cows, Vet. Rec 173 (4) (2013) 99.
[65] Z. Yue, C. Teater, Y. Liu, J. MacLellan, W. Liao, A sustainable pathway of cellulosic
ethanol production integrating anaerobic digestion with biorefining, Biotechnol.
Bioeng. 105 (6) (2010) 1031–1039.
[66] G. Markou, E. Nerantzis, Microalgae for high-value compounds and biofuels pro-
duction: a review with focus on cultivation under stress conditions, Biotechnol.
Adv. 31 (8) (2013) 1532–1542.
[67] J.N. Rogers, et al., A critical analysis of paddlewheel-driven raceway ponds for
algal biofuel production at commercial scales, Algal Res. 4 (1) (2014) 76–88.
[68] N.R. Moheimani, M.A. Borowitzka, The long-term culture of the coccolithophore
Pleurochrysis carterae (Haptophyta) in outdoor raceway ponds, J. Appl. Phycol.
18 (6) (2006) 703–712.
[69] S.R. Chia, et al., Analysis of economic and environmental aspects of microalgae
biorefinery for biofuels production: a review, Biotechnol. J. 13 (6) (2018) 1–10.
[70] S.R. Subashchandrabose, B. Ramakrishnan, M. Megharaj, K. Venkateswarlu,
R. Naidu, Mixotrophic cyanobacteria and microalgae as distinctive biological
agents for organic pollutant degradation, Environ. Int. 51 (2013) 59–72.
[71] M. Cecchin, et al., Molecular basis of autotrophic vs mixotrophic growth in
Chlorella sorokiniana, Sci. Rep., no. April (2018) 1–13.
[72] X. Liu, S. Duan, A. Li, N. Xu, Z. Cai, Z. Hu, Effects of organic carbon sources on
growth, photosynthesis, and respiration of Phaeodactylum tricornutum, J. Appl.
D. Chuka-ogwude, et al.
Phycol. 21 (2) (2009) 239–246.
[73] J. Mcgrady-steed, P.M. Harris, P.J. Morin, Biodiversity determines Ecosytem
predictability, Nature 390 (November) (1997).
[74] C. Baldisserotto, M. Giovanardi, L. Ferroni, S. Pancaldi, Growth, morphology and
photosynthetic responses of Neochloris oleoabundans during cultivation in a mix-
otrophic brackish medium and subsequent starvation, Acta Physiol. Plant. 36 (2)
(2014) 461–472.
[75] F.J. Marquez, K. Sasaki, T. Kakizono, N. Nishio, S. Nagai, Growth characteristics of
Spirulina platens & in mixotrophic and heterotrophic conditions, J. Ferment.
Bioeng. 76 (5) (1993) 408–410.
[76] F. Martínez, et al., Interactions between glucose and inorganic carbon metabolism
in Chlorella vulgaris strain, Plant Physiol. 95 (4) (1991) 1150–1155.
[77] K. Steinmüller, K. Zetsche, Photo- and metabolite regulation of the synthesis of
ribulose bisphosphate carboxylase/oxygenase and the phycobiliproteins in the
alga Cyanidium caldarium, Plant Physiol. 76 (4) (1984) 935–939.
[78] R. Kang, J. Wang, D. Shi, W. Cong, Z. Cai, F. Ouyang, Interactions between organic
and inorganic carbon sources during mixotrophic cultivation of Synechococcus sp,
Biotechnol. Lett. 26 (18) (2004) 1429–1432.
[79] R. Ramanan, B.H. Kim, D.H. Cho, H.M. Oh, H.S. Kim, Algae-bacteria interactions:
evolution, ecology and emerging applications, Biotechnol. Adv. 34 (1) (2016)
14–29.
[80] C. Marcilhac, B. Sialve, A. Pourcher, C. Ziebal, N. Bernet, B. Fabrice, Digestate
color and light intensity affect nutrient removal and competition phenomena in a
microalgal-bacterial ecosystem, Water Res. 64 (2014) 278–287.
[81] N.R. Moheimani, A. Vadiveloo, J.M. Ayre, J.R. Pluske, Nutritional profile and in
vitro digestibility of microalgae grown in anaerobically digested piggery effluent,
Algal Res. 35 (September) (2018) 362–369.
[82] L. Yang, et al., Nutrients removal and lipids production by Chlorella pyrenoidosa
cultivation using anaerobic digested starch wastewater and alcohol wastewater,
Bioresour. Technol. 181 (2015) 54–61.
[83] X. Tan, H. Chu, Y. Zhang, L. Yang, F. Zhao, X. Zhou, Chlorella pyrenoidosa culti-
vation using anaerobic digested starch processing wastewater in an airlift circu-
lation photobioreactor, Bioresour. Technol. 170 (2014) 538–548.
[84] J. Cheng, J. Xu, Y. Huang, Y. Li, J. Zhou, K. Cen, Growth optimisation of microalga
mutant at high CO2 concentration to purify undiluted anaerobic digestion effluent
of swine manure, Bioresour. Technol. 177 (2015) 240–246.
[85] C. Yan, Z. Zheng, Performance of mixed LED light wavelengths on biogas upgrade
and biogas fluid removal by microalga Chlorella sp, Appl. Energy 113 (2014)
1008–1014.
[86] A.M. Åkerström, L.M. Mortensen, B. Rusten, H.R. Gislerød, Biomass production
and nutrient removal by Chlorella sp. as affected by sludge liquor concentration, J.
Environ. Manag. 144 (2014) 118–124.
[87] L. Wang, Y. Wang, P. Chen, R. Ruan, Semi-continuous cultivation of chlorella
vulgaris for treating undigested and digested dairy manures, Appl. Biochem.
Biotechnol. 162 (8) (2010) 2324–2332.
[88] M. Singh, D.L. Reynolds, K.C. Das, Microalgal system for treatment of effluent
from poultry litter anaerobic digestion, Bioresour. Technol. 102 (23) (2011)
10841–10848.
[89] Y. Zhao, S. Sun, C. Hu, H. Zhang, J. Xu, L. Ping, Performance of three microalgal
strains in biogas slurry purification and biogas upgrade in response to various
mixed light-emitting diode light wavelengths, Bioresour. Technol. 187 (2015)
338–345.
[90] M. L. Serejo, E. Posadas, and M. A. Boncz, “Influence of biogas flow rate on bio-
mass composition during the optimization of biogas upgrading in microalgal-
bacterial processes,” 2015.
[91] M. Franchino, E. Comino, F. Bona, V.A. Riggio, Chemosphere growth of three
microalgae strains and nutrient removal from an agro-zootechnical digestate,
Chemosphere 92 (6) (2013) 738–744.
[92] S.K. Prajapati, P. Kumar, A. Malik, V.K. Vijay, Bioconversion of algae to methane
and subsequent utilization of digestate for algae cultivation: a closed loop bioe-
nergy generation process, Bioresour. Technol. 158 (2014) 174–180.
[93] F. Ji, et al., Fed-batch cultivation of Desmodesmus sp. in anaerobic digestion
wastewater for improved nutrient removal and biodiesel production, Bioresour.
Technol. 184 (2015) 116–122.
[94] F. Ji, Y. Liu, R. Hao, G. Li, Y. Zhou, R. Dong, Biomass production and nutrients
removal by a new microalgae strain Desmodesmus sp. in anaerobic digestion
wastewater, Bioresour. Technol. 161 (2014) 200–207.
[95] T. Cai, S.Y. Park, R. Racharaks, Y. Li, Cultivation of Nannochloropsis salina using
anaerobic digestion effluent as a nutrient source for biofuel production, Appl.
Energy 108 (2013) 486–492.
[96] T. Cai, X. Ge, S.Y. Park, Y. Li, Comparison of Synechocystis sp. PCC6803 and
Nannochloropsis salina for lipid production using artificial seawater and nutrients
from anaerobic digestion effluent, Bioresour. Technol. 144 (2013) 255–260.
[97] R.B. Levine, M.S. Costanza-Robinson, G.A. Spatafora, Neochloris oleoabundans
grown on anaerobically digested dairy manure for concomitant nutrient removal
and biodiesel feedstock production, Biomass Bioenergy 35 (1) (2011) 40–49.
[98] K.E. Dickinson, et al., Simultaneous remediation of nutrients from liquid anaerobic
digestate and municipal wastewater by the microalga Scenedesmus sp. AMDD
grown in continuous chemostats, J. Appl. Microbiol. 118 (1) (2015) 75–83.
[99] J. Xu, Y. Zhao, G. Zhao, H. Zhang, Nutrient removal and biogas upgrading by
integrating freshwater algae cultivation with piggery anaerobic digestate liquid
treatment, Appl. Microbiol. Biotechnol. 99 (15) (2015) 6493–6501.
[100] E. Uggetti, B. Sialve, E. Latrille, J.P. Steyer, Anaerobic digestate as substrate for
microalgae culture: the role of ammonium concentration on the microalgae pro-
ductivity, Bioresour. Technol. 152 (2014) 437–443.
[101] M. Erkelens, A.J. Ward, A.S. Ball, D.M. Lewis, Microalgae digestate effluent as a
15
Algal Research 47 (2020) 101841
growth medium for Tetraselmis sp. in the production of biofuels, Bioresour.
Technol. 167 (2014) 81–86.
[102] H.A. Abu Hajar, R.G. Riefler, B.J. Stuart, Cultivation of Scenedesmus dimorphus
using anaerobic digestate as a nutrient medium, Bioprocess Biosyst. Eng. 40 (8)
(2017) 1197–1207.
[103] E.G. Nwoba, J.M. Ayre, N.R. Moheimani, B.E. Ubi, J.C. Ogbonna, Growth com-
parison of microalgae in tubular photobioreactor and open pond for treating
anaerobic digestion piggery effluent, Algal Res. 17 (2016) 268–276.
[104] W. Mulbry, S. Kondrad, C. Pizarro, E. Kebede-Westhead, Treatment of dairy
manure effluent using freshwater algae: algal productivity and recovery of manure
nutrients using pilot-scale algal turf scrubbers, Bioresour. Technol. 99 (17) (2008)
8137–8142.
[105] J.Z. Barnett, Effects of Light Quality and Light Quantity on the Growth Kinetics of
a Louisiana Native Microalgal/Cyanobacterial Co-culture, (2015), pp. 14–17.
[106] M. Morales, J. Cabello, S. Revah, Gas balances and growth in algal cultures, in:
A. Prokop, R.K. Bajpai, M.E. Zappi (Eds.), Algal Biorefineries, 2015, pp. 263–314.
[107] M. Massa, Sustainable Production of Microalgae Biomass in Liquid Digestates and
by Products from Agro-Food Industries, (2016).
[108] J.A. Hellebust, I. Ahmad, Biological oceanography regulation of nitrogen assim-
ilation in green microalgae, Biol. Oceanogr. 5581 (1988) 241–255.
[109] G. Von Rückert, A. Giani, Effect of nitrate and ammonium on the growth and
protein concentration of Microcystis viridis Lemmermann (cyanobacteria), Rev.
Bras. Botânica 27 (2) (2004) 325–331.
[110] J.A. Raven, B. Wollenweber, L. Handley, A comparison of ammonium and nitrate
as nitrogen sources for photolithotrophs, New Phytol. 121 (1) (1992) 19–32.
[111] Q. Dortch, The interaction between ammonium and nitrate uptake in phyto-
plankton, Mar. Ecol. Prog. Ser. 61 (1990) 183–201.
[112] G. Markou, O. Depraetere, K. Muylaert, Effect of ammonia on the photosynthetic
activity of Arthrospira and Chlorella: a study on chlorophyll fluorescence and
electron transport, Algal Res. 16 (2016) 449–457.
[113] S. Boussiba, J. Gibson, Ammonia translocation in cyanobacteria, FEMS Microbiol.
Lett. 88 (1) (1991) 1–14.
[114] M. Drath, N. Kloft, A. Batschauer, K. Marin, J. Novak, K. Forchhammer, Ammonia
triggers photodamage of photosystem II in the cyanobacterium Synechocystis sp.
strain PCC 6803, Plant Physiol. 147 (1) (2008) 206–215.
[115] S. Schuldiner, H. Rottenberg, M. Avron, Determination of pH change in chlor-
oplasts, Eur. J. Biochem. 25 (1972) 64–70.
[116] A.R. Crofts, Uptake of ammonium ion by chloroplasts, and the mechanism of
amine uncoupling, Biochem. Biophys. Res. Commun. 24 (1) (1966) 127–134.
[117] P.M. Glibert, et al., Pluses and minuses of ammonium and nitrate uptake and as-
similation by phytoplankton and implications for productivity and community
composition, with emphasis on nitrogen-enriched conditions, Limnol. Oceanogr.
61 (1) (2016) 165–197.
[118] A.R. Sánchez-Rodríguez, et al., Advanced processing of food waste based digestate
for mitigating nitrogen losses in a winter wheat crop, Front. Sustain. Food Syst. 2
(July) (2018) 1–14.
[119] D.L. Sutherland, C. Howard-williams, M.H. Turnbull, P.A. Broady, R.J. Craggs, The
effects of CO2 addition along a pH gradient on wastewater microalgal photo-
physiology, biomass production and nutrient removal, Water Res. 70 (2014) 9–26.
[120] A. J. D. Ward, M. Lewis, and F. Green, “Anaerobic digestion of algae biomass: a
review,” Algal Res.., vol. 5, pp. 204–214, 2014.
[121] J.C.M. Pires, M.C.M. Alvim-Ferraz, F.G. Martins, M. Simões, Carbon dioxide cap-
ture from flue gases using microalgae: engineering aspects and biorefinery con-
cept, Renew. Sust. Energ. Rev. 16 (5) (2012) 3043–3053.
[122] A. Dimitrov, et al., A systems approach for CO 2 fixation from flue gas by mi-
croalgae — theory review, Process Biochem. 51 (2016) 1817–1832.
[123] X. Li, J. Xu, Y. Guo, W. Zhou, Z. Yuan, Effects of simulated flue gas on components
of Scenedesmus raciborskii WZKMT, Bioresour. Technol. 190 (2015) 339–344.
[124] M. Negoro, N. Shioji, Growth of microalgae in high CO2 gas and effects of SOx and
NOx, Appl. Biochem. Biotechnol. 2 (1991) 877–886.
[125] A.C. Redfield, On the proportions of organic derivatives in sea water and their
relation to the composition of plankton, University Press of Liverpool, James
Johnstone Memorial Volume (1934) 176–192.
[126] R.J. Geider, J. La Roche, Redfield revisited: variability of C:N:P in marine mi-
croalgae and its biochemical basis, Eur. J. Phycol. 37 (1) (2002) 1–17.
[127] W. a Wurts, Pond pH and Ammonia toxicity, World Aquac 34 (2) (1992) 20–21.
[128] G. Chen, L. Zhao, Y. Qi, Enhancing the productivity of microalgae cultivated in
wastewater toward biofuel production: a critical review, Appl. Energy 137 (2015)
282–291.
[129] N.R. Moheimani, M.A. Borowitzka, A. Isdepsky, S.S. Fon, Standard Methods for
Measuring Growth of Algae and Their Composition, Springer, Dordrecht
Heidelberg New York London, 2013.
[130] H. Li, Y. Tan, M. Ditaranto, J. Yan, Z. Yu, Capturing CO2from biogas plants,
Energy Procedia 114 (November 2016) (2017) 6030–6035.
[131] M. Johnson, Z. Wen, Production of oil-rich algae from animal manure using at-
tached algal culture systems written for presentation at the 2008 ASABE annual
international meeting sponsored by ASABE Rhode Island convention center ma-
terials and methods, ASABE Annu. Int. Meet. 300 (8) (2008).
[132] M.V. Jiménez-Pérez, P. Sánchez-Castillo, O. Romera, D. Fernández-Moreno,
C. Pérez-Martínez, Growth and nutrient removal in free and immobilized plank-
tonic green algae isolated from pig manure, Enzym. Microb. Technol. 34 (5)
(2004) 392–398.
[133] P.S. Lau, N.F.Y. Tam, Y.S. Wong, Wastewater nutrients removal by chlorella vul-
garis: optimization through acclimation, Environ. Technol. (United Kingdom) 17
(2) (1996) 183–189.
[134] O. Osundeko, A.P. Dean, H. Davies, J.K. Pittman, Acclimation of microalgae to
D. Chuka-ogwude, et al.
wastewater environments involves increased oxidative stress tolerance activity,
Plant Cell Physiol 55 (10) (2014) 1848–1857.
[135] J. McGrady-Steed, P.M. Harris, P.J. Morin, Biodiversity regulates ecosystem pre-
dictability, Nature 390 (6656) (1997) 162–165.
[136] J. Fargione, et al., From selection to complementarity: shifts in the causes of
biodiversity-productivity relationships in a long-term biodiversity experiment,
Proc. R. Soc. B Biol. Sci. 274 (1611) (2007) 871–876.
[137] J.C. Ogbonna, H. Yoshizawa, H. Tanaka, Treatment of high strength organic
wastewater by a mixed culture of photosynthetic microorganisms, J. Appl. Phycol.
12 (3–5) (2000) 277–284.
[138] J.C. Ogbonna, N.R. Moheimani, Potentials of exploiting heterotrophic metabolism
for biodiesel oil production by microalgae, in: N.R. Moheimani, M.P.K. de
B. McHenry, P.A. Bahri (Eds.), Biomass and Biofuels from Microalgae, 2015, pp.
45–61.
[139] S.P. Li, J.T. Li, J.L. Kuang, H.N. Duan, Y. Zeng, W.S. Shu, Effects of species richness
on cadmium removal efficiencies of algal microcosms, J. Appl. Ecol. 49 (1) (2012)
261–267.
[140] Y. Su, A. Mennerich, B. Urban, Coupled nutrient removal and biomass production
with mixed algal culture: impact of biotic and abiotic factors, Bioresour. Technol.
118 (2012) 469–476.
[141] M.A. Borowitzka, N.R. Moheimani, Open pond culture systems, in:
M.A. Borowitzka, N.R. Moheimani (Eds.), Algae for Biofuels and Energy, Springer,
Dordrecht Heidelberg New York London, 2013, pp. 133–152.
[142] K. Sompech, Y. Chisti, T. Srinophakun, Design of raceway ponds for producing
microalgae, Biofuels 3 (4) (2012) 387–397.
[143] W.J. Oswald, C.G. Golueke, Biological transformation of solar energy, Adv. Appl.
Microbiol. 2 (C) (1960) 223–262.
[144] R. Craggs, J. Park, S. Heubeck, D. Sutherland, High rate algal pond systems for
low-energy wastewater treatment, nutrient recovery and energy production, New
Zeal. J. Bot 52 (1) (2014) 60–73.
[145] P. Chen, Q. Zhou, J. Paing, H. Le, B. Picot, Nutrient removal by the integrated use
of high rate algal ponds and macrophyte systems in China, Water Sci. Technol. 48
(2) (2003) 251–257.
[146] B. Picot, H. Halouani, C. Casellas, and S. S. Moersidik, “Nutrient removal by high
rate pond system in a Mediterranean climate,” Water Sci. Technol., vol. 23, no.
March 2018, pp. 1535–1541, 1991.
[147] P. Young, M. Taylor, H.J. Fallowfield, Mini-review: high rate algal ponds, flexible
systems for sustainable wastewater treatment, World J. Microbiol. Biotechnol. 33
(6) (2017) 0.
[148] Â. Matos, W. Ferreira, L. Morioka, E. Moecke, K. França, E. Sant’Anna, Cultivation
of Chlorella vulgaris in medium supplemented with desalination concentrate grown
in a pilot-scale open raceway, Brazilian J. Chem. Eng 35 (2018) 1183–1192.
[149] G. Acien, J.M. Fernandez-Sevilla, E. Molina-Grima, Photobioreactors for the pro-
duction of microalgae, Rev. Environ. Sci. Bio/Technology 12 (2013).
[150] I. Setlik, S. Veladimir, I. Malek, Dual purpose open circulation units for large scale
culture of algae in temperate zones. Basic design considerations and scheme of a
pilot plant, Algol. Stud. für Hydrobiol (1970) 111–164 vol. Supplement.
[151] J. Doucha and K. Livansky, “Novel outdoor thin-layer high density microalgal
culture system : productivity and operational parameters novel outdoor thin-Iayer
high density microalgal culture system : productivity and operational parameters,”
Arch. Hydrobiol. Suppl. Algol. Stud., vol. 76, no. February 1995, pp. 129–147,
1995.
[152] J. Doucha, Productivity, CO 2/O 2 exchange and hydraulics in outdoor open high
density microalgal (chlorella sp.) photobioreactors operated in a middle and
southern European climate, Pp (2006) 811–826.
[153] J. Doucha, K. Lívanský, Outdoor open thin-layer microalgal photobioreactor :
potential productivity, J. Appl. Phycol. 21 (2009) 111–117.
[154] A.C. Apel, et al., Open thin-layer cascade reactors for saline microalgae production
evaluated in a physically simulated Mediterranean summer climate, Algal Res. 25
(2017) 381–390 March.
[155] M.A. Borowitzka, Commercial production of microalgae: ponds, tanks, and fer-
menters, Prog. Ind. Microbiol. 35 (C) (1999) 313–321.
[156] W. Farooq, W.I. Suh, M.S. Park, J. Yang, Water use and its recycling in microalgae
cultivation for biofuel application, Bioresour. Technol. 184 (2014) 73–81.
[157] C.U. Ugwu, H. Aoyagi, H. Uchiyama, Photobioreactors for mass cultivation of
algae, Bioresour. Technol. 99 (10) (2008) 4021–4028.
[158] J.A. Running, R.J. Huss, P.T. Olson, Heterotrophic production of ascorbic acid by
microalgae, J. Appl. Phycol. 6 (2) (1994) 99–104.
[159] L. Peng, C.Q. Lan, Z. Zhang, Evolution, detrimental effects, and removal of oxygen
in microalga cultures : a review, Environ. Prog. Sustain. Energy 32 (4) (2013)
982–988.
[160] C.B. Osmond, Some implications for the energetics of photosynthesis, Biochim.
Biophys. Acta-Rev. Bioenerg 639 (2) (1981) 77–98.
[161] C. Sousa, L. De Winter, M. Janssen, M.H. Vermuë, R.H. Wijffels, Growth of the
microalgae Neochloris oleoabundans at high partial oxygen pressures and sub-sa-
turating light intensity, Bioresour. Technol. 104 (2012) 565–570.
[162] J.C. Weissman, R.P. Goebel, J.R. Benemann, Photobioreactor design : mixing,
carbon utilization, and oxygen accumulation, Biotechnol. Bioeng. 31 (4) (1988)
336–344.
[163] Z. Arbib, J. Ruiz, P. álvarez-Díaz, C. Garrido-Pérez, J. Barragan, J.A. Perales, Long
term outdoor operation of a tubular airlift pilot photobioreactor and a high rate
algal pond as tertiary treatment of urban wastewater, Ecol. Eng. 52 (2013)
143–153.
[164] B. Molinuevo-Salces, M.C. García-González, C. González-Fernández, Performance
comparison of two photobioreactors configurations (open and closed to the at-
mosphere) treating anaerobically degraded swine slurry, Bioresour. Technol. 101
16
Algal Research 47 (2020) 101841
(14) (2010) 5144–5149.
[165] V.O. Adesanya, E. Cadena, S.A. Scott, A.G. Smith, Life cycle assessment on mi-
croalgal biodiesel production using a hybrid cultivation system, Bioresour.
Technol. 163 (2014) 343–355.
[166] R.R. Narala, et al., Comparison of microalgae cultivation in photobioreactor, open
raceway pond, and a two-stage hybrid system, Front. Energy Res. 4 (AUG) (2016)
1–10.
[167] M.E. Huntley, et al., Demonstrated large-scale production of marine microalgae for
fuels and feed, Algal Res. 10 (2015) 249–265.
[168] W. Blanken, M. Janssen, M. Cuaresma, Z. Libor, T. Bhaiji, R.H. Wijffels, Biofilm
growth of Chlorella sorokiniana in a rotating biological contactor based photo-
bioreactor, Biotechnol. Bioeng. 111 (12) (2014) 2436–2445.
[169] M. Gross, Z. Wen, Yearlong evaluation of performance and durability of a pilot-
scale revolving algal biofilm (RAB) cultivation system, Bioresour. Technol. 171
(2014) 50–58.
[170] M. Gross, D. Jarboe, Z. Wen, Biofilm-based algal cultivation systems, Appl.
Microbiol. Biotechnol. 99 (14) (2015) 5781–5789.
[171] Y.H. Lin, J.Y. Leu, C.R. Lan, P.H.P. Lin, F.L. Chang, Kinetics of inorganic carbon
utilization by microalgal biofilm in a flat plate photoreactor, Chemosphere 53 (7)
(2003) 779–787.
[172] L.B. Christenson, R.C. Sims, Rotating algal biofilm reactor and spool harvester for
wastewater treatment with biofuels by-products, Biotechnol. Bioeng. 109 (7)
(2012) 1674–1684.
[173] M.B. Johnson, Z. Wen, Development of an attached microalgal growth system for
biofuel production, Appl. Microbiol. Biotechnol. 85 (3) (2010) 525–534.
[174] M. Gross, W. Henry, C. Michael, Z. Wen, Development of a rotating algal biofilm
growth system for attached microalgae growth with in situ biomass harvest,
Bioresour. Technol. 150 (2013) 195–201.
[175] E. Eroglu, R.S. Wijihastuti, E. Grenik, A. Vadiveloo, N.R. Moheimani, X. Lou,
Application of poly(2-hydroxyethyl methacrylate) hydrogel disks for the im-
mobilization of three different microalgal species, J. Chem. Technol. Biotechnol.
93 (10) (2018) 2887–2897.
[176] J.A. Gerde, L. Yao, J.Y. Lio, Z. Wen, T. Wang, Microalgae flocculation: impact of
flocculant type, algae species and cell concentration, Algal Res. 3 (1) (2014)
30–35.
[177] A. Ozkan, H. Berberoglu, Cell to substratum and cell to cell interactions of mi-
croalgae, Colloids Surfaces B Biointerfaces 112 (2013) 302–309.
[178] F. Berner, K. Heimann, M. Sheehan, Microalgal biofilms for biomass production, J.
Appl. Phycol. 27 (5) (2015) 1793–1804.
[179] Y. Shen, H. Zhang, X. Xu, X. Lin, Biofilm formation and lipid accumulation of
attached culture of Botryococcus braunii, Bioprocess Biosyst. Eng. 38 (3) (2015)
481–488.
[180] D. Hoh, S. Watson, E. Kan, Algal Biofilm Reactors for Integrated Wastewater
Treatment and Biofuel Production: A Review, 287 Elsevier B.V, 2016.
[181] J.C. Ogbonna, H. Yada, H. Tanaka, Effect of cell movement by random mixing
between the surface and bottom of photobioreactors on algal productivity, J.
Ferment. Bioeng. 79 (2) (1995) 152–157.
[182] D.J. Dye, Spatial Light Dilution as a Technique for Conversion of Solar Energy to
Algal Biomass, Dissertations (2010), p. 142.
[183] E.A. Laws, K.L. Terry, J. Wickman, M.S. Chalup, A simple algal production system
designed to utilize the flashing light effect, Biotechnol. Bioeng. 25 (10) (1983)
2319–2335.
[184] C.K. Powell, J.B. Chaddock, J.R. Dixon, The motion of algae in turbulent flow,
Biotechnol. Bioeng. 7 (1965) 295–308.
[185] R.L. Miller, A.G. Fredrickson, A.H. Brown, H.M. Tsuchiya, Hydromechanical
method to increase efficiency of algal photosynthesis, Ind. Eng. Chem. Process.
Des. Dev. 3 (2) (1964) 134–143.
[186] J. Huang, et al., Investigation on the performance of raceway ponds with internal
structures by the means of CFD simulations and experiments, Algal Res. 10 (2015)
64–71.
[187] Q. Zhang, S. Xue, C. Yan, X. Wu, S. Wen, W. Cong, Installation of flow deflectors
and wing baffles to reduce dead zone and enhance flashing light effect in an open
raceway pond, Bioresour. Technol. 198 (2015) 150–156.
[188] R. Voleti, Experimental Studies of Vertical Mixing in an Open Channel Raceway
for Algae Biofuel Production, All Grad. Theses Diss (2012).
[189] N.R. Moheimani, M.A. Borowitzka, Limits to productivity of the algae
Pleurochrysis carterae (Haptophyta) grown in outdoor raceway ponds, Biotechnol.
Bioeng. 96 (1) (2007) 27–36.
[190] J. Myers, J.-R. Graham, On the mass culture of algae II. Yield as a function of cell
concentration under continous sunlight irradiance, Plant Physiol. 34 (3) (1959)
345–352.
[191] J. Myers and J. Graham, “On the mass culture of algae. III. Light diffusers; high vs
low temperature Chlorellas,” Plant Physiol.., vol. 36, no. 3, pp. 342–346, 1960.
[192] A.M. Mayer, U. Zuri, Y. Shain, H. Ginzburg, Problems of design and ecological
considerations in mass culture of algae, Biotechnol. Bioeng. VI (1964) 173–190.
[193] H. Takano, et al., CO2 removal by high-density culture of a marine cyano-
bacterium Synechococcus sp. using an improved photobioreactor employing light-
diffusing optical fibers, Appl. Biochem. Biotechnol. 34 (1992) 449–458.
[194] S. Fatemeh, B. Richards, N. Willoughby, Bioresource technology spectral conver-
sion of light for enhanced microalgae growth rates and photosynthetic pigment
production, Bioresour. Technol. 125 (2012) 75–81.
[195] H.D. Amrei, R. Ranjbar, S. Rastegar, Using fluorescent material for enhancing
microalgae growth rate in photobioreactors, J. Appl. Phycol. 27 (1) (2015) 67–74.
[196] E. Sforza, E. Barbera, A. Bertucco, Improving the photoconversion ef fi ciency : an
integrated photovoltaic-photobioreactor system for microalgal cultivation, Algal
Res. 10 (2015) 202–209.
D. Chuka-ogwude, et al.
[197] L. Wondraczek, et al., Photosynthetic activity in algae reactors, Nat. Commun. 4
(May) (2013) 1–6.
[198] J.C. Ogbonna, T. Soejima, H. Tanaka, An integrated solar and artificial light
system for internal illumination of photobioreactors, J. Biotechnol. 70 (1–3)
(1999) 289–297.
[199] M. Raeisossadati, N.R. Moheimani, D. Parlevliet, Luminescent solar concentrator
panels for increasing the efficiency of mass microalgal production, Renew. Sust.
Energ. Rev. 101 (October 2018) (2019) 47–59.
[200] Z. Yang, J. Cheng, K. Li, J. Zhou, K. Cen, Optimizing gas transfer to improve
growth rate of Haematococcus pluvialis in a raceway pond with chute and oscil-
lating baffles, Bioresour. Technol. 214 (2016) 276–283.
[201] J. Cheng, W. Guo, C. Cai, Q. Ye, J. Zhou, Alternatively permutated conic baffles
generate vortex flow field to improve microalgal productivity in a raceway pond,
Bioresour. Technol. 249 (September 2017) (2018) 212–218.
[202] C.U. Ugwu, J.C. Ogbonna, H. Tanaka, Improvement of mass transfer character-
istics and productivities of inclined tubular photobioreactors by installation of
internal static mixers, Appl. Microbiol. Biotechnol. 58 (5) (2002) 600–607.
[203] J. Cheng, Z. Yang, Q. Ye, J. Zhou, K. Cen, Improving CO2 fixation with microalgae
by bubble breakage in raceway ponds with up-down chute baffles, Bioresour.
Technol. 201 (2016) 174–181.
[204] E. Koutra, G. Grammatikopoulos, M. Kornaros, Selection of microalgae intended
for valorization of digestate from agro-waste mixtures, Waste Manag. 73 (2018)
123–129.
17
Algal Research 47 (2020) 101841
[205] L.M. González-González, D.F. Correa, S. Ryan, P.D. Jensen, S. Pratt, P.M. Schenk,
Integrated biodiesel and biogas production from microalgae: towards a sustainable
closed loop through nutrient recycling, Renew. Sust. Energ. Rev. 82 (May 2017)
(2018) 1137–1148.
[206] B. Kotzen, M.G.C. Emerenciano, N. Moheimani, G.M. Burnell, Aquaponics: alter-
native types and approaches, Aquaponics Food Prod. Syst. (2019) 301–330.
[207] Y. di Chen, S.H. Ho, D. Nagarajan, N. qi Ren, J.S. Chang, Waste biorefineries —
integrating anaerobic digestion and microalgae cultivation for bioenergy pro-
duction, Curr. Opin. Biotechnol. 50 (2018) 101–110.
[208] R. Fornarelli, P.A. Bahri, N. Moheimani, Utilization of Microalgae to Purify Waste
Streams and Production of Value Added Products, North Sydney (2017).
[209] B. Rincón, M. José, D. de la L.-C. Fernández-Rodríguez, R. Borja, The influence of
microalgae addition as co-substrate in anaerobic digestion processes, Intech Open
2 (2018) 64.
[210] J. Kim, C.M. Kang, Increased anaerobic production of methane by co-digestion of
sludge with microalgal biomass and food waste leachate, Bioresour. Technol. 189
(2015) 409–412.
[211] L. Riosa, N. Sasongkoa, P. Bahrib, M. Filhoc, A. Vadiveloo, N.R. Moheimani,
Preliminary Economic Assessment of Integrating Microalgae Cultivation Systems
in Existing Piggeries for the Treatment of ADPE, (2018).
[212] T.S. Severin, A.C. Apel, T. Brück, D. Weuster-Botz, Investigation of vertical mixing
in thin-layer cascade reactors using computational fluid dynamics, Chem. Eng.
Res. Des. 132 (2018) 436–444.