Science of The Total Environment

Science of the Total Environment 704 (2020) 135303
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Science of the Total Environment

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Cultivating microalgae in wastewater for biomass production, pollutant

removal, and atmospheric carbon mitigation; a review
Ayesha Shahid b,1, Sana Malik b,1, Hui Zhu a, Jianren Xu c, Muhammad Zohaib Nawaz d,e, Shahid Nawaz f,
Md. Asraful Alam g,⇑, Muhammad Aamer Mehmood a,b,⇑
a
School of Bioengineering, Sichuan University of Science and Engineering, Zigong 643000, People’s Republic of China
b
Bioenergy Research Centre, Department of Bioinformatics & Biotechnology, Government College University Faisalabad, Faisalabad 38000, Pakistan
c
College of Bioscience and Engineering, North Minzu University, Yinchuan 750021, Ningxia, China
d
State Key Laboratory of Marine Environmental Science, Institute of Marine Microbes and Ecospheres, College of Ocean and Earth Sciences, Xiamen University, Xiamen, China
e
Department of Computer Science, The University of Agriculture Faisalabad, Faisalabad 38000, Pakistan
f
Department of Chemistry, The University of Agriculture Faisalabad, Faisalabad 38000, Pakistan
g
School of Chemical Engineering, Zhengzhou University, Zhengzhou 450001, China
h i g h l i g h t s g r a p h i c a l a b s t r a c t
Microalgae are the most promising

photoautotrophs to fix atmospheric
carbon.
Requirement of huge amounts of
freshwater to culture microalgae is
challenging.
Alternatively, wastewater cultivation
offers low-cost biomass production.
Wastewater nutrient stress can
manipulate the microalgal metabolite
content.
Mixed cultivation offers additional
benefits of efficient wastewater
treatment.
a r t i c l e i n f o a b s t r a c t
Article history: Water shortage is one of the leading global problems along with the depletion of energy resources and
Received 7 August 2019 environmental deterioration. Recent industrialization, global mobility, and increasing population have
Received in revised form 27 October 2019 adversely affected the freshwater resources. The wastewater sources are categorized as domestic, agricul-
Accepted 29 October 2019
tural and industrial effluents and their disposal into water bodies poses a harmful impact on human and
Available online 22 November 2019
animal health due to the presence of higher amounts of nitrogen, phosphorus, sulfur, heavy metals and
Guest Editor: Hafiz M. N. Iqbal other organic/inorganic pollutants. Several conventional treatment methods have been employed, but
none of those can be termed as a universal method due to their high cost, less efficiency, and non-
Keywords:
environment friendly nature. Alternatively, wastewater treatment using microalgae (phycoremediation)
Microalgae cultivation offers several advantages over chemical-based treatment methods. Microalgae cultivation using wastew-
Wastewater treatment ater offers the highest atmospheric carbon fixation rate (1.83 kg CO2/kg of biomass) and fastest biomass
Biorefineries productivity (40–50% higher than terrestrial crops) among all terrestrial bio-remediators with concomi-
CO2 fixation tant pollutant removal (80–100%). Moreover, the algal biomass may contain high-value metabolites
Cost-effective including omega-3-fatty acids, pigments, amino acids, and high sugar content. Hence, after extraction
of high-value compounds, residual biomass can be either directly converted to energy through thermo-
chemical transformation or can be used to produce biofuels through biological fermentation or transes-
terification. This review highlights the recent advances in microalgal biotechnology to establish a
⇑ Corresponding authors at: School of Bioengineering, Sichuan University of Science and Engineering, Zigong 643000, People’s Republic of China (M.A. Mehmood).
E-mail addresses: [email protected] (Md. Asraful Alam), [email protected] (M.A. Mehmood).
1
First two authors contributed equally to this paper and should be considered as co-first authors.
https://doi.org/10.1016/j.scitotenv.2019.135303
0048-9697/Ó 2019 Elsevier B.V. All rights reserved.
2 A. Shahid et al. / Science of the Total Environment 704 (2020) 135303
biorefinery approach to treat wastewater. The articulation of wastewater treatment facilities with
microalgal biorefinery, the use of microalgal consortia, the possible merits, and demerits of phycoreme-
diation are also discussed. The impact of wastewater-derived nutrient stress and its exploitation to mod-
ify the algal metabolite content in view of future concerns of cost-benefit ratios of algal biorefineries is
also highlighted.
Ó 2019 Elsevier B.V. All rights reserved.
1. Introduction alternative replacing conventional treatment methods due to its

vast availability, higher nutrient consumption ability and diverse
Dawn of the 21st century led the world towards increasing applications of the algal biomass produced (Lam et al., 2012).
urbanization, industrialization and commercialization at the cost This review summarizes different wastewater treatment meth-
of increasing carbon emission, depleting energy and water ods and focused on cost-effective and efficient microalgae-based
resources, and contamination of water bodies with toxic pollutants treatment of wastewater (phycoremediation) along with the
(Khan et al., 2019). It is expected that the world’s population will potential problems and opportunities (Fig. 1). It also highlights
increase from 6.3 billion in 2015 to approximately 9 billion in the possibilities of exploiting the wastewater as a low-cost growth
2050 (Ng et al., 2017). The increased population would require media and as a natural stress-manipulative strategy for enhanced
enough and cleaner energy supply as well as the clean water biomass productivity and algal metabolite content, presenting an
resources. To acquire and maintain a clean environment, it would algal-biorefinery concept.
be needed to reduce CO2 content by 50–80% with an increase of
50% in water and energy resources respectively (Hightower and
Pierce, 2008; Ng et al., 2017). According to 2014 statistics, esti- 2. Microalgae-based wastewater treatment
mated global freshwater consumption was 3700 billion m3 (Diniz
et al., 2017), where most of it is being converted into wastewater Algae are one of the most diverse groups of photosynthetic
due to human activities. Based on its origin, wastewater produced organisms starting from simple blue-green algae (cyanobacteria/
by human activities is termed as domestic, aqua-cultural, agricul- prokaryotes) to complex sea-weeds and kelps. On average, more
tural or industrial sewage/effluents (Diniz et al., 2017). Various than 350,000 microalgal species have been discovered (Shahid
industries including paper and pulp industry, sugarcane industry, et al., 2017). In general, they are believed to contain as high as
textile or tannery industry, and pharmaceutical industry (Lv 70% lipids, 60% carbohydrates and 65% of proteins and essential
et al., 2017; Ramlow et al., 2017) contribute to surface water pol- amino-acids respectively (Afzal et al., 2017). Microalgal biomass
lution causing water scarcity. Polluted and untreated water con- is an alternative of traditional feedstocks (Khan et al., 2018)
taminates freshwater resources by releasing excess amounts of because microalgae have a short growth cycle when compared to
nitrogen and phosphorus which enhances eutrophication and terrestrial plants or energy crops, higher biomass productivity,
ecosystem destruction, making it unsuitable for human consump- higher harvesting index, and the highest rate of carbon fixation.
tion (Godfray et al., 2010; Morée et al., 2013). Water pollution Additionally, microalgae don’t require large arable land instead
(acidification, eutrophication, sewage, heavy metals and other can be grown on marginal lands by using seawater or wastewater
organic pollutants) (Godfray et al., 2010) have confirmed harmful as growth media (Miranda et al., 2017). Microalgae play a vital role
effects on human health, including growth inhibition, feminization in environmental carbon mitigation and bioremediation due to
of male organisms, carcinogenicity, (Butkovskyi et al., 2017) devel- their higher photosynthetic efficiency (40–50% higher than terres-
opment of waterborne diseases like diarrhea, typhoid, intestinal trial plants) (Chen et al., 2015) and remarkable CO2 sequestration
worms, gastroenteritis, Cryptosporidium infections, cardiovascular, (1 kg of microalgae consumes 1.83 kg of CO2 and accounts for
renal failure and hypertension (Daud et al., 2017), both in devel- 40% of global CO2 sequestration) (Chisti, 2007; Ng et al., 2017).
oped and developing countries. Microalgae can also be used as bioindicators to detect the climate
The main aim of wastewater treatment is to remove the excess changes in aquatic environments (O’Neill et al., 2019) and can con-
amount of micropollutants (Grandclement et al., 2017), nutrients sume wastewater nutrients (80–100% uptake of nitrogen and phos-
(nitrogen, sulfur, copper, phosphorus) (Wang et al., 2017a), heavy phorus) for high productivities of biomass and value-added
metals (copper, zinc, lead, mercury, chromium, nickel, cadmium) products (Grandclement et al., 2017; Miranda et al., 2017; Su
(Bilal et al., 2013) and organic pollutants (phenolic compounds, et al., 2016). Depending upon the microalgal strains, they can be
aromatic hydrocarbons, biocides, surfactants, antibiotics etc.) from employed in various industries like cosmetics, poultry, biofertiliz-
wastewater (Salama et al., 2017). A variety of chemicals, physical ers, medicine and green-fuels namely bioalcohols, biogas and bio-
and biological wastewater treatment methods have been diesel (Afzal et al., 2017). However, it is required to develop cost-
employed (Wang et al., 2017a) while the biological approach being effective strategies to produce cost-competitive algal products,
more common (Grandclement et al., 2017) to remove these pollu- because at present the algal biofuels cannot compete the prices
tants. Depending on the effluent requirement, the wastewater of the fossil fuels (Dasan et al., 2019). Hence, selection of appropri-
treatment method is selected (Dvořák et al., 2014). However, there ate strain (Gill et al., 2016), use of low cost media, optimization of
is no standalone method that can be applied to a variety of efflu- conditions for higher biomass production, cell stoichiometry to
ents because of the limitations associated with each method divert the balance towards target product, suitable commercializa-
(Table 1). In general, conventional treatment methods have short- tion, and reducing the operational cost (mainly associated with
comings such as the requirement of large land, intensive energy cultivation and harvesting stages) are focused aspects of the algal
input, and extensive maintenance and operational costs research (Ng et al., 2017). Fig. 2 summarizes a roadmap of microal-
(Udaiyappan et al., 2017). Hence, it is required to develop alterna- gal growth optimization and strain development for microalgal
tive technologies to recycle wastewater along with the fixation of biorefinery.
atmospheric carbon (Hariz and Takriff, 2017). Microalgae-based Wastewater is the most suitable resource for algal biomass pro-
bioremediation is the safest, promising, and the most efficient duction because of several reasons such as; (i) cheaper growth
A. Shahid et al. / Science of the Total Environment 704 (2020) 135303 3
Table 1
Overview of the conventional and modern wastewater treatment methods.
Treatment process Type Principle Pollutant Removal Merits Demerits References

efficiency
Filtration Micro-filtration, Removal of domestic, 99% (dyes Easy operation, cost- Filter may get clog, (Eyvaz et al.,
Ultra-filtration, solids (>5– industrial and and TC) effective, Remove Poor micro-pollutant 2017;
Reverse osmosis, 20 mm) by pigment rich 74% (TN) suspended solid, removal, membrane Udaiyappan
Nano-filtration passing liquid wastewater 77% (COD) alkalinity, organic and fouling, high et al., 2017;
through porous inorganic contaminants, operational cost Wang et al.,
membrane high quality treated 2017)
water
Adsorption Activated carbon or Selective Industrial, 96% Easy operation, no Low selectivity, (Crini et al.,
aluminum, zeolites, separation agricultural, (organic additional chemicals, difficult maintenance, 2019; Guo
organic polymers, through binding domestic and pollutants) cost-effective, high metal formation of waste et al., 2019)
of pollutant on Heavy metal binding capacity products
absorbent containing
surface wastewater
Coagulation Chemical, electro, Dissociation and Heavy metals, >70% COD, Ecofriendly, lower Identification of (Mohd-
natural- material hydrolysis of Textile, 90–100% operational cost, efficient commercial scale-up Salleh et al.,
based coagulant into petroleum, (Heavy pollutant removal, parameters, electrode 2019;
positive ions; cosmetics metals) energy efficient passivation, higher Sillanpää
reactive to wastewater maintenance et al., 2018)
negative collides
Advance oxidation Electrochemical, Formation of Recalcitrant 53–96% Degradation of organic Partial degradation, (Affam et al.,
Ultrasound-based, organic pollutant organic (COD), 21– pollutants, effective, vast expensive, presence of 2018;
Plasma, ozonation, removing pollutants, 85% (TOC) applicability, oxidize toxic products Miklos et al.,
UV-radiation, reactive industrial and odor compounds 2018)
photo-catalytic oxidizing species pesticidal
wastewater
Adsorption, Depends on Pollutant Industrial 88–92% High efficiency, energy- Challenging scale-up (Ejraei et al.,
membrane- membrane and removal by serial wastewater, (COD), 91– saving, increased 2019)
filtration and nanoparticles being treatment organic 98% (TS), membrane performance,
photo-catalytic employed pollutants 85–91% less fouling
degradation (Detergents)
(Hybrid)
Filtration and Chemical Filtration of Phenolic 92% (TS), High treatment High maintenance cost, (Enaime
coagulant- coagulants wastewater compounds, 36% (COD), efficiency, Energy saving et al., 2019)
flocculation followed by organic 81% (Fatty
(Hybrid) treatment by pollutants, Matter)
coagulating suspended
flocculant solids,
Nano-materials Magnetic, Act as absorbent Heavy metals, 90–100% High efficiency and Eco-concern, high cost, (Gautam
carbonated, metal- for the inorganic, (various adsorption capacity, poor recyclability, et al., 2019;
oxide photolytic organic & metals) compatible with other toxicity Sadegh
degradation of emerging techniques et al., 2017)
pollutants pollutants,
petrochemicals
Biogenic Nano- Bacteria, Fungi, Reduction or Radio-active 75–99% Eco friendly, non-toxic, Instability, tricky (Ali et al.,
particles Algae plant excreted oxidation of contamination, (Dyes), 66– cost-effective, recovery of 2019;
bioactive molecules metals by inorganic and 85% (Heavy sustainable, energy intracellularly Gautam
-based natural organic metals) efficient synthesized et al., 2019)
chemicals-based pollutant nanoparticles
nanoparticles
Microbial electro- Microbial-fuel cell, Oxidation or Recalcitrant >25–63% Wide applicability, Difficult scale-up with (Mohan
chemical Microbial- reduction of matter, (COD) production of electricity cost-effective & et al., 2019)
Technology electrochemical cell, pollutants by industrial, and other valuable efficient performance
Bio-electrochemical respiring domestic and commodities
treatment, microbes food-processing
Microbial wastewater
electrolysis
Biochar Biomass (algae, crop Act as catalysts Phenolic 65–99% High efficiency, robust, Low removal efficiency (Huang
residues), industrial or absorbent to compounds, (dyes), economical, large specific of raw-biochar, some et al., 2019)
by-products, degrade or heavy metals, >90% area, high porosity, less types may contain
municipal waste remove the dyes, organic & (phenols) energy consuming toxins or metals, non-
pollutant inorganic ecofriendly production
contaminants process
Biological method Autotrophic & Assimilation and Nitrates, >90% (COD), Economical, high bio- Slow, requires constant (Ahmad
heterotrophic dissimilation of phosphates, 38–90% degradability, efficient maintenance, low et al., 2019;
microbes (Bacteria, pollutants dairy waste (Nitrogen) elimination of pollutants applicability, Crini and
Fungi etc) compromised Lichtfouse,
performance due to 2019)
abiotic factors
(continued on next page)

Table 1 (continued)
Treatment process Type Principle Pollutant Removal Merits Demerits References

efficiency
Biomass Algae, Uptake of Industrial, 22–98% High pollutant removal, Compromised (Molinuevo-
Cyanobacteria nutrients for domestic (TP), energy & cost efficient, performance due to Salces et al.,
biomass and wastewater, 20–100% eco-friendly, biorefinery- abiotic factors and 2019)
metabolite heavy metals, (TN), >90% based process wastewater
production dyes, organic & (COD) characteristics, difficult
inorganic harvesting, large area
pollutants requires
Fig. 1. Merits and demerits of algal biomass production and processing in algal biorefinery.
media, (ii) support bulk biomass and biofuel production, (iii) can wastewater (Lin et al., 2017). Chlorella variabilis showed to con-
supply ample nutrients, and (iv) offers the possibility of integrating sume nutrients from textile effluents and with 100% remediation
algal cultivation with the existing infrastructure wastewater treat- ability for nickel, aluminum, and iron with biomass productivity
ment (Roostaei and Zhang, 2016). Several studies have been con- of 74 gm 2 d 1 with lipid yield of 20% (Bhattacharya et al.,
ducted in last decades on microalgae-based phycoremediation of 2017). Similarly, high nitrogen (99.6%) and phosphorus (91.2%)
wastewater (Chen et al., 2015; Salama et al., 2017; Udaiyappan removal efficiency with the concomitant production of biomethane
et al., 2017; Wang et al., 2017a) and biorefinery based approaches (523 mL) was reported by C. vulgaris grown in municipal wastew-
have been proposed (Gill et al., 2013). Microalgae have been stud- ater (Calicioglu and Demirer, 2017). Freshwater microalgae includ-
ied for wastewater (industrial and domestic) treatment including ing Cladophora glomerata and Oedogonium westii can remove heavy
brewery wastewater (Ferreira et al., 2017), domestic wastewater metals from industrial wastewater and showed 80% of cadmium
(Calicioglu and Demirer, 2017), textile wastewater (Wu et al., and 66% of nickel accumulation, respectively (Khan et al., 2017).
2017a), pharmaceutical waste streams (Xie et al., 2019), slaughter- Additionally, Neochloris aquatica CL-M1 was employed to produce
house industry (Aziz et al., 2019), heavy metal-containing wastew- butanol along with wastewater treatment (Wang et al., 2017c),
ater (Khan et al., 2017), palm oil mill effluents (Hariz and Takriff, where biobutanol yield of 0.89 g L 1 h 1 with 96.2% of NH3-N
2017), starch-containing textile wastewater (Lin et al., 2017), and removal efficiency was observed. Moreover, lipid-rich Botryococcus
agro-industrial wastewater (Jayakumar et al., 2017). Though sp. removed 59.9% nitrogen, 36.8% phosphate and 54.5% organic
microalgae-based remediation has numerous benefits, however, carbon along with the production of 72.5% of crude oil content,
there are several challenges that also need to be addressed. when cultivated in domestic wastewater (Gani et al., 2017).
Several studies have demonstrated species of Chlamydomonas, Biotic factors (microbial load / competing pathogens) and abi-
Chlorella and Scenedesmus can be employed for efficient nutrient otic factors (nutrients, pH, and CO2) play a pivotal role in microal-
uptake (N, P) (Gao et al., 2016) and removal of toxic pollutants gal metabolism. Manipulation of stress factors including biotic
and heavy metals (Khan et al., 2017; Matamoros et al., 2015) from and/or abiotic through wastewater significantly affects the produc-
wastewater. Ankistrodesmus along with Scenedesmus and Chlorella tivities of both biomass and product of interest (Table 2). Unravel-
has shown to degrade organic pollutants present in paper and oil ing the underlying processes and reorienting the related pathways
mill industry wastewater (Bhattacharya et al., 2017). Similarly, Sce- can greatly contribute to achieving robustness, enhanced produc-
nedesmus sp. represented higher utilization efficiency of 98.2%, tivities in energy and cost-efficient manner (Chen et al., 2017).
97.1% and 95.2% for butyrate, propionate, and acetate respectively Utilization of wastewater as an alternative media offers additional
with a growth rate of 0.53 gd 1 when cultivated in textile desizing benefits including wastewater cleaning, recycling, reducing the
Fig. 2. Road map of steps involved in strain development and process optimization.
environmental pollutions, and provision of low-cost growth media 141.5 mgL 1day 1 of protein productivities were reported C.
(Yadav et al., 2019). However, it requires detailed studies of using sorokiniana cultured in wastewater (Guldhe et al., 2017). Cultivat-
wastewater as low-cost growth media and studying the impact of ing C. vulgaris in mixed piggery and brewery wastewater reduced
biotic and abiotic factors to attain the full potential of microalgae nitrogen and ammonia by 96% and 100%, respectively producing
for the biorefinery. 2.85 gL 1 biomass (Zheng et al., 2018). Similarly, COD and nitrogen
removal efficiencies of 76% and 98%, respectively, were reported
for wastewater treatment using S. obliquus (Gupta et al., 2016).
2.1. Removal of macro and micro-nutrients
These studies have clearly indicated that nitrogen stress has a
global impact on various microalgae to enhance lipid content,
Microalgae store lipids as polar (polyunsaturated fatty acids)
but it cannot be applied on a commercial scale using synthetic
and non-polar forms (saturated fatty acids, mainly in the form of
growth media, which will raise the cost. Alternatively, nitrogen
triacylglycerides) which are important to maintain membrane
stress can be applied using wastewater, which often has higher
functions or to perform other cellular activities. These lipids can
nitrogen content (municipal wastewater), however, wastewater
be transesterified to produce biodiesel (Paliwal et al., 2017). The
from industrial sources may have lower nitrogen content. Conse-
stress of various macro and micronutrients, mainly nitrogen and
quently, water from these sources can be used to exert nitrogen
phosphorus, has been studied widely to enhance algal metabolite
stress on the microalgae. Removal of nitrogen by microalgae does
content mainly lipids.
not only treat wastewater but also trigger the accumulation of
value-added products. However, aore detailed studies are required
2.1.1. Nitrogen in the future to elucidate the role of wastewater derived N-stress
Nitrogen is one of the principal nutrients for the synthesis of on growth and biomass productivity of microalgae.
nucleic acid, protein, energy-carrying molecules (ATP), and
enzymes (Juneja et al., 2013). Naturally, nitrogen is available in
the form of nitrate, urea, ammonium, and peptones (Minhas 2.1.2. Phosphorus
et al., 2016). In microalgae, nitrogen accounts for 1–20% of dry cell Phosphate is another important (second only to nitrogen)
matter and is part of the essential functional and structural pro- macronutrient of a living system which is part of RNA, DNA back-
teins of algae (Juneja et al., 2013). Nitrogen starvation has been bone, ATP, phospholipids (Juneja et al., 2013), phosphoproteins,
considered as the most effective induction strategy (Shi et al., polyphosphates and in the form of NADPH. Phosphate limiting
2017) that shifts the organism’s metabolic pathway towards conditions lead to organic carbon accumulation (TAG) and
enhanced lipid synthesis, triglyceride accumulation, protein con- decreased cell division. Phosphorus deficiency is also known to
tent reduction and increased carotenogenesis, at the expense of affect the energy-requiring processes like protein synthesis, tran-
biomass production (Juneja et al., 2013; Minhas et al., 2016). scription, and carbon cycle (Mühlroth et al., 2017). Generally, it
An increase of 2.27-fold in lipid content was observed in Scene- constitutes <1–1% of the total dry mass of microalgae (Minhas
desmus quadricauda when grown under nitrogen-starved condi- et al., 2016). The C. protothecoides has shown to accumulate
tions (226 mgL 1) (Anand and Arumugam, 2015). Acutodesmus 32.8% of lipid content under mixotrophic conditions using wastew-
dimorphus accumulated 75% neutral lipids of total lipids under ater as growth media which was deficient in phosphorus (Li et al.,
nitrogen-starvation conditions (Chokshi et al., 2017). Cultivation 2014). Similarly, under nutrient stress, the C. vulgaris was shown to
of Pseudokirchneriella subcapitata under nitrate stress conditions accumulate lipids by 17.41% producing 9.81 gL 1 of biomass, which
resulted in 160 mgL 1d 1 fatty acid accumulation (Del Río et al., is comparatively low than nitrogen and sulfur stress (Sakarika and
2017). Scenedesmus obliquus showed 4.4 mgL 1day 1 of total nitro- Kornaros, 2017). Similarly, 53% of lipid content and 23.45 mgL 1 of
gen removal efficiency with 1.4 gL 1 of biomass and 29.8 mgL 1- lipid productivity was reported for Chlorella under phosphorus
day 1 of lipid productivity when grown on urban wastewater deprivation conditions (Wong et al., 2017).
(Álvarez-Díaz et al., 2017). Similarly, removal of 84.51% of nitrate Phycoremediation of municipal wastewater by Micractinium sp.
and 75.56% of ammonium along with the production of 172.9 IC-76 resulted in 77% of PO4-P removal efficiency with 37.18 mg
mgL 1day 1 of carbohydrate, 150.2 mgL 1day 1 of lipid and L 1day 1 of biomass productivity and 36% of lipid content
Table 2
Impact of wastewater derived nutrients on the production of biomass and metabolite contents with the focus on microalgal phycoremediation and biorefinery ability.
Microalgae Wastewater Wastewater- Nutrient removal (%) Biomass Metabolites (%) References
derived productivity
Total Total Chemical Lipid Protein Carbs/
stress (mgL 1d 1)
Nitrogen Phosphorus Oxygen others
demand
Scenedesmus Brewery Low pH, 88 30 71 64 (bio-oil) 31.4 0.2–1 (Ferreira et al.,
obliquus effluent high mgmL 1 2019)
nutrient and (Phenol)
sugars
Tetraselmis suecica Dairy High 83 100 – 42.5 – – 11.7 (Daneshvar
Nutrient, mgL 1 et al., 2019)
varying pH (Chl-a)
Tribonema minus Tofu-whey High 92.8 72 86.7 431.6 37 15.5 31 (Wang et al.,
nutrients 2019a,b)
and COD
Ecuadorian Synthetic High 52–93 67 – 0.6–1.8 28 – – (Benítez et al.,
Chlorella sp. (Secondary nutrients, 2019)
effluent) alkaline
C. pyrenoidosa Olive-oil High organic – 97 96.2 1.25 23 11 65 (Malvis et al.,
mill matter 2019)
C. sorokiniana Cooking Organic 29.4 46 89 85.7 23.3 39.3 29.4 (Li et al.,
cocoon pollutant, 2019a,b)
high protein
Scenedesmus sp. Meat High N and P 90 85 – 98.5 23.2 41.2 – (Apandi et al.,
market 2019)
1 1
Chlorella sp. Soybean- Moderate 85 97 70.5 – 7.22 mgL d – 2.86 (Qiu et al.,
processing nitrates mgL 1d 1
2019)
(diluted)
Ascochloris sp. Raw-Dairy High N and P 80 97 96 94–98 33.4 – – (Kumar et al.,
2019)
Chlorella & Oocystis Power plant Sulfate rich 22–32 (Sulfates) 50–25.24 Reported biodiesel potential (Mohammadi
sp. (Respectively) et al., 2018)
Dunaliella salina Tertiary Moderate 57.5 69 52 28.25 – – – (Liu and Yildiz,
treated Nitrate and P 2018)
municipal
C. sorokiniana Diluted High nitrates 84.2 47 – 1524 62.4 mg/g 388.2 mg/ 11.82 mg/ (De Francisci
municipal & and (FAME) g g (chloro- et al., 2018)
industrial phosphate phyll)
Chlorella sp. MM3 Diluted Low pH, 89.3 56.5 – 4.4x106 cells/ 51 – – (Ganeshkumar
winery & high organic mL et al., 2018)
piggery matter &
(80:20) nutrients
Desmodesmus sp. Synthetic High P and 85 (Ni) >90 94 (Cu) 0.05 17.6 – – (Rugnini et al.,
industrial heavy 2018)
effluent metals
C. vulgaris Aqua- High carbon 76.5 92.7 75.5 187 9.07 47.5 19.09 (Daneshvar
culture and & nutrient et al., 2018)
pulp
1
Chalymondomonas Palm oil High 65 34 56 – 90 mgg – – (Hazman et al.,
sp. mill effluent nutrient and 2018)
(POME) CO2
Ascochloris sp. Raw-dairy High 78 98 95 102–207 34 – – (Kumar et al.,
(ADW007) nutrients 2018)
Dunaliella Diluted food High >80 80 – 200 37 (SFA) – – (Wu et al.,
tertiolecta leachate nutrients 2018)
Coelastrum sp. Cattle farm High 80 100 42 281 50.7 – – (Mousavi et al.,
nutrients 2018)
Chlorella sp. Domestic- High 82 (Zn), 80 (Mn), 56 (Cu) 50 43.8 – – (Mishra et al.,
(ISTLA) treatment nutrients 2018)
plant
Tetraselmis chuii Aqua- High 54 – – 3.25x105 17.6 33 12 (Khatoon et al.,
culture nutrients cells/mL 2018)
Dunaliella sp. Synthetic High 93.6 (Ni) – 65 pgcell – 0.97 (Moussa et al.,
1
amount of mgg 2018)
heavy
metals
1 1
Tetraselmis sp Synthetic High 90 – 80 124.5 29.48 mg d – – (de Alva et al.,
mariculture nutrients 2018)
and solids
Parachlorella Agro-waste High >98 59 39 62 23.8 (FA) – – (Koutra et al.,
kessleri nutrients 2018)
Asterarcys Municipal Nutrients 48 50 – 65 21.9 – 50 (Odjadjare
quadricellulare wastewater et al., 2018)
treatment
plant
Table 2 (continued)
Microalgae Wastewater Wastewater- Nutrient removal (%) Biomass Metabolites (%) References
derived productivity
Total Total Chemical Lipid Protein Carbs/
stress (mgL 1d 1)
Nitrogen Phosphorus Oxygen others
demand
S. obliquus Secondary Low pH and 94 – 74 200 – 50 – (Marchão et al.,
brewery high 2018)
effluent nutrient
S. acuminatus Paper and High pH and 100 >97 – 685 19.9 24.3 60.5 (Tao et al.,
pulp nutrients 2017)
C. vulgaris Swine High solids 71 54 78.7 157 17.4 58.8 9.1 (Deng et al.,
manure and 2017)
ammonium
Desmodesmus sp. Oil-refinery Acidic, high – 53 82 270 22 – – (Mar et al.,
(Dilute) COD & 2016)
phosphate,
greases
1
Chlorella Sea-food High 94.5 68.4 – 77.7 27 – 39 mgL (Gao et al.,
processing nutrients Chloro- 2018)
phyll
(Piligaev et al., 2017). Cultivation of Desmodesmus abundans on the potential of pollutant removal, biomass and metabolite pro-
synthetic wastewater showed 16% of lipid content and 87.52% of ductivities under sulfur stress alone, and/or the combined stress
phosphate removal rate (Prasad et al., 2017). Treatment of sewage of other nutrients, which may lead towards the selection of suit-
water by phosphate starved Scenedesmus (Yewalkar-Kulkarni et al., able strains. While the selection of strain will be influenced by
2017) resulted in an enhanced carbohydrate ratio with 87% of the type and source of the wastewater too.
phosphate removal. Hence, it is suggested to expose the microalgae
to the combined stress of nitrogen and phosphorus to achieve 2.1.4. Heavy metals
higher biomass and lipid productivities (Chen et al., 2017). A suit- Metals are the natural constituents of soil and earth crust. How-
able cost-effective alternative is the use of wastewater. Cultivation ever, in ecological terms, any metalloid or metal which has bioac-
of microalgae in wastewater will consume phosphorus (act as cumulation ability and causes environmental pollution is termed
stress factor) and thus help in wastewater treatment. as heavy metal. Some of the metals are micronutrients (Cu, Zn,
Ni, Mn, and Co) and are essential for growth (Kumar et al., 2015),
2.1.3. Sulfur and some others like Mn, Cu, I, Zn, Fe, Pb, etc. are proven to be ben-
Sulfur is also one of the most important macronutrients. Com- eficial for nutritional quality improvement and other important
monly, sulfate is consumed as a sulfur source by plants and algae. functions of living system (Wells et al., 2017). Some heavy metals
Cellular processes namely assimilation, secondary metabolic path- including Pb, Cd, Cr, and Hg have unidentified biological functions
ways, oxidative stress responses, flavonoid, and nitrogen metabo- and are toxic in nature (Afshan et al., 2015; Kumar et al., 2015) as
lism are affected by sulfur. In algae, enhanced assimilation of their excessive uptake may affect metabolic processes, the physical
Sulfur is believed to downregulate the photosynthesis, and its structure of algae and can cause toxicity, mutagenesis and aller-
stress induces expression of stress-associated proteins (Giordano genicity (Mikulewicz et al., 2017).
and Raven, 2014). Naturally, sulfate is present in excessive Heavy metals stimulate the ROS (reactive oxygen species) for-
amounts in the wastewater from paper and pulp industry, pharma- mation resulting in oxidative damage. Decreased metabolite con-
ceutical industry, mining, and food processing (Lv et al., 2017). An tent (pigments, proteins, and monosaccharides), size and number
increasing trend in neutral lipids (123–172%), oligosaccharide, TAG of cells observed to be related to lead accumulation in Acutodesmus
and polysaccharide levels was observed for wild-type Chlorella obliquus (Piotrowska-Niczyporuk et al., 2015). Increased protein
strain cultivated under sulfur-deprived conditions (Cakmak et al., and carbohydrate ratios were observed when C. sarokiniana culti-
2012). Moreover, the sulfur starvation showed to increase the b- vated in mixotrophic and photoautotrophic conditions under the
carotene level from 6.753 mgL 1 to 14.616 mgL 1 with decreasing influence of titanium-dioxide (TiO2) nanoparticles (Marchello
biomass production in Dunaliella salina (Shaker et al., 2017). Unlike et al., 2018). Exposure of copper sulfate (CuSO4) induced lipid per-
Nitrogen, Sulfur starvation has proven to be more efficient for oxidation due to the formation of ROS and reduced the levels of
starch accumulation when compared to Nitrogen starvation which carotenoids, chlorophyll-a, and b in Chlorella, which reflects highly
causes lipid accumulation (Vitova et al., 2015). An increase of 18- toxic nature of CuSO4 (Wan et al., 2018). Cheng and coworkers
fold in starch content was observed in C. reinhardtii when cultured (Cheng et al., 2016) reported 71%, 93% and 74% reduction in caro-
under S-deprived conditions. It is believed that sulfur starvation tenoids, chlorophyll-a, and chlorophyll-b level, respectively, in C.
inhibits energy-consuming pathways like cell growth and division vulgaris as a result of 7 mgL 1 cadmium treatment while ~96%
while, shifting the pathways towards starch accumulation (Antal increase in soluble protein accumulation was observed.
et al., 2014). Interestingly, Sulfur deprivation altered the fatty acid Modern agronomic practices (metal-based pesticides), intense
composition of C. lobophora (Takeshita et al., 2014). On the other industrialization (metal, textile, mining etc.), enhanced anthro-
hand, sulfate stress negatively affected the pollutant removal abil- pogenic activities (rubber, paint, paper, and metal alloys production),
ity, growth and self-flocculation efficiency of Chlorococcum sp. GD and unauthorized waste disposal have increased the concentration of
when grown in synthetic municipal wastewater (Lv et al., 2017). these pollutants in environment (Das and Osborne, 2018; Kumar and
It indicates that the impact of sulfate may not be global, hence Gunasundari, 2018). Biosorption of heavy metals from wastewater
we need to conduct carefully designed detailed studies to evaluate by microalgae is a promising alternative as it is a cost-effective,
ecologically safe and efficient method (Ummalyma et al., 2018) when oleoabundans, pH 9.5 supported maximum cell growth (1.04
compared to conventionally employed methods. C. vulgaris, Chlamy- gL 1), lipid content (151.2 mgg 1) and lipid productivity (19.1
domonas reinhardtii, Chlorococcum spp, Phaeodactylum tricornotum, mgL 1day 1) under oxygen stress (Peng et al., 2017). S. abundans
Scenedesmus quadricauda, Spirogyra spp. and many other algal species was able to tolerate a large range of pH (5–8) however, pH 8 was
have been reported for heavy metal biosorption from wastewater optimum to obtain the highest growth rate of 769 mgL 1 and pH
(Brinza et al., 2007; Ummalyma et al., 2018). Biosorption studies of 6 favored lipid concentration to 179 mgL 1 (Mandotra et al.,
Scenedesmus sp. showed the potential of said species to remove heavy 2016). Similarly, pH alteration enhanced the self-flocculation abil-
metals namely Cu (73–98%), Zn (65–98%), Cr (81–96%) and Pb (75– ity of Dunaliella sp. when 2 or 6 N NaOH was added in the culture
98%) from tannery wastewater under laboratory conditions (Ajayan media (Byrd and Burkholder, 2017). These studies indicated that
et al., 2015). Similarly, the biomass of Chara aculeolate removed Cd, pH manipulation can be employed to enhance the algal metabolite
Pb, and Zn via biosorption at the rate of 23 mgg 1, 105.3 mgg 1 and content and biomass productivity by outcompeting the pathogens.
15.2 mgg 1 respectively from municipal wastewater (Sooksawat However, more detailed studies are required to elucidate the
et al., 2016). Moreover, S. armatus and C. vulgaris showed bioaccumu- impact of wastewater-derived pH on biomass productivity and
lation efficiency for Cd2+ and Pb2+ by 89.96% and 88.98%, respectively metabolite content.
(Zabochnicka-Świa˛tek and Rygała, 2017). Similarly, Cladophora glom-
erate and Oedogonium westii showed the removal of Cd and Ni by 80%
and 66.3%, respectively from industrial wastewater (Khan et al., 2017). 3. Binary culture to enhance phycoremediation of wastewater
Interesting results were obtained for self-flocculating microalga C. vul-
garis JSC-7 which was able to remove Cd and Zn (60–80% respectively) It is difficult to maintain pure cultures under field conditions,
more efficiently as compared to the non-flocculating similar strain. which is even more difficult when using ponds receiving wastew-
Moreover, an increase in the photosynthetic pigments and growth ater. Hence, recently researchers focused on the cultivation of
was observed under heavy metal stress, showing its excellent heavy mixed cultures. Binary cultures in the form of consortia
metal tolerance ability (Alam et al., 2015). (microalgae-microalgae or microalgae-bacteria) have been
Heavy metal accumulation is associated with toxicity and ROS reported extensively for enhanced wastewater treatment due to
production where Pb, Cu, Cd, and Ti greatly reduce the growth their higher nutrient removal ability with enhanced biomass pro-
and pigment content of microalgae. However, in some cases, an duction (Table 3). Polycultures allow us to develop robust biologi-
increase in the protein and lipid content was also observed. Heavy cal systems for wastewater treatment as they can be combined
metal-containing wastewater poses many adverse effects and is with various metabolic processes to enable themselves to survive
not suitable for human consumption. Phycoremediation of heavy under environmental stress conditions. Moreover, integrated con-
metal-containing wastewater is an eco-friendly and cost-effective sortia can uptake nutrients at a higher rate (Johnson and
approach owing to the remarkable potential of microalgae to Admassu, 2013; Rawat et al., 2011; Renuka et al., 2013) because
remove high levels of heavy metals from wastewater. one strain can remove nitrogen and another can remove heavy
metals specifically. These consortia have several advantages
2.2. Impact of pH including (i) contamination and predator resistances due to pro-
duction of allelochemicals (ii) enhanced nutrient consumption;
Invasion of pathogenic microbes (predators or competitors) in ensuring sufficient nutrient supply during whole process, (iii)
the open pond cultivation of microalgae causes contamination of development of settleable system for flocculation thus, eliminating
microalgae and poses a major challenge during cultivation. There limitations of harvesting, and (iv) enhanced viability of phycore-
are several factors that can influence the load of invading organ- mediation; as loss of one microbe is compensated by other species.
isms. For instance, microalgae may produce some extracellular However, it faces some constraints as it’s difficult to develop robust
compounds to inhibit the competing organisms resultantly domi- consortia as a variety of combinations are possible. Moreover,
nating the environment. Some secretory metabolites can even help maintenance of consortia for longer periods especially in an
the microalgae to modify the pH of the media (Shahid et al., 2019) open-pond system proven to be challenging (Gonçalves et al.,
which helps to outcompete the invading organisms. Hence, pH is 2017).
one of the most important parameters which can be employed to
inhibit or outcompete the invading organisms. Alteration in pH
has been reported to improve culture densities by decreasing the 3.1. Microalgae-bacteria (MB) consortia
microalgal contaminants (Bartley et al., 2014). Additionally, pH
plays a vital role in algal cultivation as it is responsible for nutrient The symbiotic relationship of microalgae and bacteria may be in
and CO2 availability and solubility. Moreover, it is known to affect the form of commensalism, mutualism or parasitism. In general,
the activity of various enzymes to enhance the triglyceride accu- bacteria heterotrophically produce CO2 and other important nutri-
mulation (Juneja et al., 2013; Ying et al., 2014). Optimum pH for ents that are consumed by microalgae for their growth (Zhu et al.,
microalgae cultivation usually ranges from 7.0 to 7.6 (neutral 2019). In return, oxygen produced by microalgae during photosyn-
pH) but, pH tolerance is species-specific and maximum biomass thesis is valuable for bacteria (Rashid et al., 2018). Moreover, bac-
productivities for S. obliquus and Ettlia sp. were observed at pHs teria provide growth-promoting hormones and vitamin B to
7.0 and 8.5, respectively (Chen et al., 2017). The pH of the growth microalgae which are necessary for growth (Fuentes et al., 2016).
media influences the microbial enzyme activity and solubility of Additionally, this symbiotic relationship protects the microalgae
environmental micro-pollutants. Therefore, pH variation determi- from other invading species. On the other hand, bacteria can dam-
nes the fate of pollutants during bioreactor treatments. Further- age the microalgal cell wall to utilize intracellular nutrient
more, acidic to neutral pH values are significant for improved (Magdouli et al., 2016). This property is of special interest during
pharmaceutical degradation (Grandclement et al., 2017). harvesting stages where cell rupturing is required to obtain the
Cultivation of C. vulgaris at pH ranging from 3 to 11 represented desired product thus, reducing cost and time of downstream pro-
its ability to act differently under specific pH as highest biomass cessing in the biorefinery. The MB-consortia also consume the dead
productivity (0.541 days 1) and lipid content of 53% was observed algal cells as a nutrient source (Ramanan et al., 2016). Excretion of
at pH 7.5 while, pH 9.5 found to be suitable for cell aggregation special chemicals by bacteria and microalgae may also suppress
(Sakarika and Kornaros, 2016). Interestingly, in the case of N. the growth of each other (López-Serna et al., 2019). This property
Table 3
Exploitation of binary cultures for the wastewater treatment and production of value-added products.
Type of Consortia Cultivation mode Wastewater Nutrient Biomass Impact on References

consortia source removal (%) production metabolites
(gL 1) (mgL 1)
Algal-bacteria Chlorella, Klebsiella & Co-cultivation in Dairy Farm 84.7 2.87 – (Makut et al.,
Acinetobacter automated bioreactor (Nitrates) 90 2019)
(COD)
Algal-bacteria Chlorella, Klebsiella & Co-cultivation in Synthetic 93.5 (nitrates) 2.84 – (Makut et al.,
Acinetobacter automated bioreactor 82 (COD) 2019)
Algal-bacteria C. vulgaris & activated Co-cultivation Municipal 55–64 (COD) 1.1–1.0.42 17.4–22% (lipid) (Leong et al.,
sludge 2019)
Algal-bacteria Chlorella, Scenedesmus & Symbiotic system Synthetic 100 (COD & 0.76 15.24–16.67% (lipid) (Chen et al.,
activated sludge municipal PO4 3-P) 2019)
sewage 98 (NH+4-N)
Algal-bacteria C. sarokiniana, Light-limiting Synthetic 98 (N) 2.5 – (Fan et al.,
Nitrosomonas & heterotrophic municipal 88 (COD) 2020)
Dechloromonas 96 (P)
Algal-bacteria Desmodesmus sp. & Algae-based co- Piggery 52 (NH+4-N) – 4.74 chlorophylls (Wang et al.,
nitrifying-bacteria cultivation 100 (TP) 2019a,b)
Algal-bacteria C. vulgaris & Aerobic-illuminiation Synthetic 80 (Ni) – – (Batool et al.,
Exiguobacterium (metal-rich) 79 (Cu) 2019)
profundum 56.4 (Cr)
Algal-bacteria Chlorella, Klebsiella & Batch mode Photo- Paper industry 99.9 (TN) 3.17 15% crude oil (Goswami
Acinetobacter bioreactor 95 (COD) et al., 2019)
Algal-bacteria Spongiochloris & Airlift bioreactor Petroleum 97 (COD) 8.51 338 chlorphyll-a, 2.92 (Abid et al.,
Hydrocabonoclastic 99 gL 1day 1 CO2 fixation 2017)
(hydrocarbon)
Algal-bacteria Scenedesmus & aerobic- Photo illumination Coke 100 (TN) – 32–40 FAME (Ryu et al.,
heterotroph (Petroleum) 90 (phenol) 2017)
Algal-bacteria Scenedesmus Two-phase Municipal 98 (TP) 1.8 22.6% lipid (Lee et al.,
Flavobacteria & photoperiodic 96 (TN) 2016)
Sphingobacteria 92 (COD)
Algal-fungal Scenedesmus obliques & Non-sterile Municipal 96 (nitrates) 2.74 2200 (Walls et al.,
wild yeast heterotrophic 100 (TAN) bio-ethanol 2019)
Algal-fungal C. vulgaris & Aspergillus – Synthetic 47.4 (TN) 0.65 59% lipids (Hultberg
niger pharmaceutical et al., 2019)
Algal-fungal C. pyrenoidosa & Pilot-scale bioreactor Piggery 83 (TN) 1.0 60% protein (Li et al.,
Rhodotorula glutinis 53 (TP) 2019a,b)
85 (COD)
Algal-fungal Chlorella vulgaris & Co-culture fermenter Starch 80 (COD) 9.8 12.34 carotenoids (Zhang et al.,
Rhodotorula glutinis 85 (organic 2019)
acids)
Algal-fungal Scenedesmus & Non-sterile Seafood 74 (COD) 2.17–6.64 600–1700 lipids (Srinuanpan
Trichoderma ressei processing 93 (TP) et al., 2018)
44 (TN)
Algal-fungal C. vulgaris & Yarrowia Photo-bioreactor Yeast industry 80 (NH3-N & 1.23–1.56 183 lipids (Qin et al.,
lipolytica COD) 2018)
Algal-fungal C. vulgaris & Ganoderma CO2 supplementation Biogas slurry 68 (COD) 644.3 – (Zhou et al.,
lucidu (Photo-bioreactor) 61.7 (TN) 2018)
64 (TP)
Algal-fungal C. vulgaris, Ganoderma Photobioreactor Biogas slurry 72–73 (TN & 0.41 Improve biogas by 89% (Wang et al.,
lucidum TP) CO2 2017b)
Algal-algal Chlorella & Scenedesmus Symbiotic system Synthetic 100 (COD & 0.05–0.7 15–18% lipid (Chen et al.,
municipal Nitrate) 2019)
sewage 95 (PO4 3-P)
Algal-algal Wild-algae & – Simulated 87 (Nitrate) 0.278 11.5% lipid (Qu et al.,
Scenedesmus municipal 19 (P) 2019)
1 1
Algal-algal Chlorella & Scenedesmus Thin-layer reactor Anaerobically 98 2.96 5.4 mgL d lipid (Raeisossadati
digested Piggery (Ammonia) et al., 2019)
44 (COD)
Algal-algal Leptolyngbya & Non-aseptic Cheese whey 70 (nitrate) 0.9 124 algal oil (Tsolcha et al.,
Ochromonas 93 (COD) 2018)
84 (P)
Algal-algal Mixed algal phylum Heterotrophic Whey – 14.32 1910 lipid (Jordaan et al.,
processing 2018)
Algal-algal Mixed algal phylum Sterile-heterotrophic Fish cannery – 14.02 1240 lipid (Jordaan et al.,
2018)
Algal-algal Leptolyngbya & Mixotrophic Winery & raisin 93 (COD) 1.3 13% lipids (Tsolcha et al.,
Ochromonas 78 (TN) 2017)
99 (P)
Algal-algal Native algal consortia Pilot-scale (raceway Greywater 99.7 (nitrate) 0.7 45.8% lipid, (Kumar et al.,
pond) 99 (TP) 28% protein, 10% carbs 2017)
Algal-algal C. zofingiensis, Photo-autotrophic Dairy 91–95 (TP) 5.1–5.4 143–150 (Qin et al.,
Scenedesmus & Chlorella 57–62 (COD) mgL 1d 1 lipids 2016
(continued on next page)

Table 3 (continued)
Type of Consortia Cultivation mode Wastewater Nutrient Biomass Impact on References

consortia source removal (%) production metabolites
(gL 1) (mgL 1)
Algal-algal Native microalgae Photo-autotrophic Livestock 80–100 (all 1.93 54% proteins, (Choudhary
consortia nutrients) 31 lipids, et al., 2016)
10% carbs
Algal-algal Chlorella, Scenedesmus, High-rate algal pond Dairy farm 98 (COD) 153.54 29,470 Lha 1yr 1
(Hena et al.,
1 1
Chlamydomonas (HARP) Ton ha yr Algal oil 2015)
can be useful to reduce sterilization cost as it eliminates the con- association can act as a self-sufficient organization to improve
tamination chances (Kouzuma and Watanabe, 2015). the overall performance and economics of the integrated microal-
The MB-consortia have shown to be effective for removal of gal industry at large scale (Ummalyma et al., 2017). Additionally,
phosphorus (35–88%), nitrogen (43–89%) and carbon (59–80%) fungal pellets may act as natural coagulants and ultimately helping
respectively from municipal wastewater in a lab-scale photobiore- the microalgal flocculation, hence making harvesting easier. These
actor (Lee et al., 2015). Moreover, a marine algal-microbial (Pic- pellets also have the potential of treating wastewater by entrap-
ochlorum sp, Pseudomonas sp., and Chitrinomycetes) consortium ping sludge solids (Ummalyma et al., 2017). Furthermore, 30% of
was developed for the treatment of marine aquaculture effluents the total fungal biomass consists of lipids, making them suitable
which showed up to 95% of removal efficiency in 4–5 h biodiesel producer candidates (Zhou et al., 2013).
(Babatsouli et al., 2015). Improvement in total phosphorus and The mixed culture of C. vulgaris and Mucor indicus reduced the
total nitrogen removal by 46% and 12% from domestic wastewater phosphate and total ammonia and nitrogen (TAN) to almost unde-
was observed in batch reactors cultivated with the MB-consortia tectable levels from synthetic aquaculture wastewater. This pro-
(Tang et al., 2016). The MB-consortium based on B. licheni- cess also enabled the flocculation of 860 mg DW of myco-algal
formis + C. vulgaris showed excellent efficiency to remove COD biomass (Barnharst et al., 2018). Biogas up-gradation and domestic
(86.5%), TN (88.9%) and TP (80.2%) from synthetic wastewater (Ji sewage wastewater treatment were simultaneously performed by
et al., 2018). Similarly, the symbiotic relationship of Chlorella and algal-fungal co-cultivation which removed TP and COD by 81% (Xu
Proteobacteria removed 72% TN in an outdoor cultivation system et al., 2017). Similarly, co-cultivation of C. vulgaris with Ganoderma
while 100% TP and 83% Zn removal efficiency were observed in lucidum reduced TP, TN and COD concentrations by 84%, 74%, and
an indoor cultivation system using piggery wastewater (García 79% respectively from swine wastewater treatment. Moreover, an
et al., 2017). association of P. subcapitata and G. lucidum successfully removed
CO2 with 84% efficiency for biogas up-gradation (Guo et al.,
3.2. Microalgae-microalgae consortia 2017). These studies have clearly demonstrated that myco-algal
associations have the potential to enhance the wastewater treat-
In order to minimize the issues and challenges regarding the ment potential and fungal pellets can contribute towards easier
microalgal cultivation, one promising alternative is to cultivate harvesting of the algal biomass. However, detailed studies are
multiple algal species which have a synergistic impact on one required to evaluate the impact of myco-algal associations on the
another to enhance the production and productivities as diverse metabolite content of the microalgae. Because the presence of
communities may enhance biomass specific lipid production when fungi in the culture media can substantially modify the extracellu-
compared to corresponding monocultures (Stockenreiter et al., lar and intracellular algal metabolites which may improve or even
2016). Additionally, diversity correlates with the biomass stability lower the content of any desired molecule. Moreover, the fungal
which is an important requirement of mass cultivation (Nalley pellets may also interfere with the post-harvesting processing of
et al., 2014). Moreover, a prodigious variety of traits by primary the algal biomass for the extraction of any desired organic
producer communities relates to higher diversity (Stockenreiter compounds.
et al., 2016).
More than 96% of nutrient removal efficiency along-with 6.82% 4. Carbon dioxide fixation
lipid content and 9.2–17.8 tonnes year 1ha 1 of biomass produc-
tivity was achieved using polyculture of 15 native-algal strains According to 2014 statistics, the total emission of CO2 was 6870
(Chinnasamy et al., 2010). Mixed microalgal cultures predomi- MMT (Million metric tons), equivalent to 81% of the world’s GHG
nantly consisting of Chlorella with small amounts of Scenedesmus emission (Wilbanks and Fernandez, 2014) and major global warm-
could remove 31 mgL 1 of phosphorus and 481 mgL 1 of nitrogen ing contributor. Industrial processes contributed to 21% of GHG
from textile wastewater when cultivated under photoautotrophic emissions (Cheah et al., 2015). Microalgae are believed to have
conditions (Huy et al., 2018). Polyculture of Chlorella sp. displayed the potential to fix the atmospheric carbon at the highest rate
the ability to removal 100% nitrates from swine wastewater and when compared with any other photosynthetic system (Gill
accumulated high lipid and protein content in the ratio of 59% et al., 2016, 2013). Algae have been extensively studied for GHG
and 34% respectively. However, lipid content only accounts for mitigation by reducing the CO2 content in biosphere through pho-
3% of total biomass content (Michelon et al., 2016). tosynthetic fixation (Abid et al., 2017). Their CO2 sequestration effi-
ciency is 10–50 times higher than terrestrial plants (Abid et al.,
3.3. Myco-algal consortia 2017; Cheng et al., 2013). Microalgae can convert CO2 from indus-
trial gas and atmosphere into high chemical energy-containing
Naturally, microalgae live in association with fungi in the form organic biomass like carotenoid, bioethanol, acetone and lipids
of lichens. This strategy benefits both partners; fungi obtain essen- (Zhu et al., 2017). Different microalgae namely S. obliquus, C.
tial nutrients and sugars from algae and in return provide protec- pyrenoidosa, C. reinhardtii, Chlorococcum littorale, and D. terteolacta
tion to microalgae from abiotic stress. It is proposed that this have shown the ability of HCO3 1 and CO2 utilization because they
harbor external carbonic anhydrase (Zhou et al., 2017). Immobi- directly by fermenting high carbohydrate (>40%) containing algal
lized Nannochloropsis sp. Mitigated >99% CO2 in secondary POME strains. Algal species like Chlamydomonas, Spirulina, Euglena, Chlor-
(Palm Oil Mill Effluent) with concomitant lipid production of ella, Scenedesmus, and Dunaliella have been extensively studied for
0.35 gL 1 lipid production which was 1.41-fold higher when com- bioethanol production. Various studies indicated the potential of
pared to the control (Cheirsilp et al., 2017). Cultivation of S. obli- wastewater grown algae to accumulate carbohydrates (Mehar
quus in beer wastewater supplemented with 5% CO2 promoted et al., 2019). Residual biomass (lipid-free, carbohydrate rich) can
cell growth and lipid accumulation (Wu et al., 2017b). also be utilized for bioethanol fermentation (Shahid et al., 2019)
Microalgae-based sludge treatment reduced CO2 emission by 22– and doesn’t require laborious pretreatments as the case with plant
54% and 43–103% during the whole year and in summer, respec- biomass. Carbohydrate content of algae can also be used to pro-
tively (Nordlander et al., 2017). Phycoremediation of palm oil mill duce bio-butanol, bio-methane, biogas, and syngas.
secondary effluents by immobilized Nannochloropsis sp.
showed > 99% CO2 mitigation efficiency (Cheirsilp et al., 2017).
5.2. Algae as high-value nutraceutical/health supplement
The CO2 content may manipulate the algal metabolite content.
For instance, higher fatty acid content was achieved in C. rein-
Some algal strains tend to produce health related FA like
hardtii, S. obliquus, C. minutissima, and D. tertiolecta by exposing
omega-3, omega-6 and docosahexaenoic acid (DHA) as major
them to enhanced CO2 concentrations (Zhu et al., 2017). In another
algal-based FA. They are non-toxic and more stable as compared
study, involving eight locally isolated microalgal strains, cultiva-
to fish DHA (Kumar and Singh, 2019). Cyanobacteria and algae
tion was conducted under 20% CO2 feeding (Hussain et al., 2017),
are the natural sources for carotenoids and diverse carotenoids
and maximum biomass production of 1.4 gL 1 for strain UMN268
including astaxanthin and lutein. Production of these compounds
was observed and it was correlated with nutrient uptake. Exposure
can be enhanced through abiotic factor manipulation. Wastewater
of Asterarcys quadricellulare and C. sarokiniana to high levels of CO2
grown algae can be utilized for this purpose and provides a cost-
resulted in an increase in carbohydrate content of total dry cell
effective sustainable alternative. Astaxanthin has vast applications
mass by 55–71% (Varshney et al., 2018). Similarly, S. bajacaliforni-
in medical sciences due to its anti-oxidant, anti-inflammatory,
cus supplemented with 25% CO2 accumulated lipid and carbohy-
anti-cancer, and anti-aging properties. Moreover, it also improves
drate by 25.81% and 26.19%, respectively (Patil and Kaliwal,
the nervous system, respiratory system, fertility, and digestive sys-
2017). These studies have clearly indicated that CO2 concentration
tem. Wastewater integrated algal-growth has been suggested for
can manipulate the content and the composition of the algal
improved astaxanthin production. This impact has been reviewed
metabolites and this manipulation may be employed to achieve
in detail by Shah et al., (Shah, 2019). Similarly, other carotenoids
the desired metabolite content in selected microalgal strains. How-
have shown various nutraceutical properties. Cyanobacteria (group
ever, the impact of CO2 content derived from wastewater (the sol-
of algae) produce large amounts of industrially and nutraceutically
uble form of CO2) needs to be carefully evaluated in future through
important compounds called phycobilins (Pancha et al., 2019)
wastewater-oriented studies because wastewater from different
which are colored protein-pigment complexes having antimicro-
sources may have different levels of soluble CO2 depending upon
bial, anticancer, and antioxidant properties. They can also be used
nature, geographic position and origin of the wastewater. Fig. 3
to produce protein-rich energy drinks and can be applied has food
shows a schematic diagram of microalgal cultivation and process-
colors.
ing as a carbon neutral process.
Wastewater-cultivated algae could be used as animal feed,
biofertilizer, and cosmetic agents. Biochar produced by algal pyrol-
5. Wastewater integrated algal-biorefinery for bioproducts ysis is rich source of nutrients and can be utilized as biofertilizer in
agriculture. Spirulina, Chlorella, Euglena, Tetraselmis, Synechococcus,
Circular bio-economy is an emerging concept, focusing on the Nannochloropsis have been utilized for human consumption as well
sustainable production, conversion, and utilization of renewable as aquaculture and animal feed supplement due to their high pro-
resources into value-added products. Photosynthetic organisms tein content and nutritional value (Shahid et al., 2020). Algal
such as microalgae are the focal point in developing closed-loop extracts have been widely used in cosmetic industry as skin and
systems due to their eco-friendly and versatile properties. hair protectants due to their anti-oxidant, anti-irritant, anti-
Wastewater integrated closed-biorefinery contributes to process aging, sun-protecting and tissue regenerating abilities. Chondrus,
economy and sustainability by resource recovery and by reducing Chlorella, Dunaliella, Nannochloropsis, Spirulina have been widely
the ecological footprint (Javed et al., 2019; Mohan et al., 2019). utilized for commercial cosmetic products (Javed et al., 2019;
Wastewater cultivated algae are rich source of primary (carbohy- Shahid et al., 2020). Fig. 4 shows production and processing of algal
drates, proteins, lipids) and secondary (pigments, anti-oxidants) biomass to produce diverse products in an algal biorefinery.
metabolites that could be exploited to produce biofuels, bio-
polymers, biofertilizers, nutraceuticals, food/health grade com-
6. Conclusion, prospects and recommendations
pounds, enzymes, feed supplements etc. and the treated wastewa-
ter can be reutilized for the agricultural or industrial purposes
Microalgae are a remarkable biological resource to produce bio-
(Mohan et al., 2019).
fuels and value-added products at industrial scale in an eco-
friendly manner. However, the cost associated with algal biomass
5.1. Algae as fuel source production and processing questions the commercial viability of
the process. Fortunately, microalgal cultivation in wastewater
Algae are known to accumulate 30–80% of lipids which nor- offers a promising alternative to deal with the higher operational
mally consist of 90–95% of triacylglycerides. Wastewater cultiva- cost. Because wastewater does not only provide a low-cost growth
tion is a cost-effective method to enhance biomass production media for algal cultivation but also provides cost-benefits associ-
and to modify lipid content and fatty acid (FA) composition. Most ated with the wastewater treatment. Moreover, the unbalanced
of the algal strains such as Chlorella produce FA ranging from C16- ratios of nutrients on the microalgae may exert abiotic stresses
C18 which are suitable for biodiesel production; similar in proper- on algal biomass diverting the metabolic pathways to produce
ties to traditional fossil-based diesel. Ethanol is another important either more protein or more lipids and pigments which may add
fuel and a chemical source. It can be produced from syngas or additional value. In this regard, a biorefinery approach is feasible
Fig. 3. Schematic representation of carbon neutral nature of microalgal cultivation and processing.
Fig. 4. Overview of microalgal biomass production and processing in an integrated microalgal biorefinery to produce a variety of products in a multi-product algal
biorefinery.
where a spectrum of marketable products may be obtained from industrial robustness in algal biorefineries. Keeping in view the
the single process. Wastewater is a major global problem espe- progress made in algal research, recent scenario and prospects,
cially in heavily populated areas and must be recycled or treated the following recommendations are made to achieve commercial
before disposal. On the other hand, wastewater is a rich source robustness.
of nutrients and consumption of these nutrients by microalgae
(phycoremediation) not only enhance productivities of biomass Cultivation: the microalgal cultivation systems need to be
but other value-added products (lipids, pigments, proteins, carbo- improved by developing low-cost growth media or using
hydrates, etc.). Moreover, the nutrient removal efficiency of wastewaters as growth media to reduce the cost. Bioprospect-
microalgae can be enhanced by applying binary cultures that ing is required to isolate indigenously successfully adapted
may consist of microalgae-microalgae, microalgae-bacteria or strains for regional or territorial applications. The strains
microalgae-fungi associations. These associations also improve adapted to grow at odd pH values (low or high) may be selected
the flocculation ability while avoiding the contamination chances to outcompete the contaminating microbes at large-scale
and may improvise the natural metabolite content of microalgae. cultivation.
However, detailed studies are required in the future to study the Harvesting: harvesting involves 20–30% cost in the algal bio-
impact of wastewater-derived stress on the biomass productivity mass production and processing which can be lowered by
of consortia and the post-harvesting processing of the biomass developing robust harvesting techniques. Bio-flocculation and
along with the metabolite content. Moreover, stress-responsive self-flocculation seem attractive harvesting approaches. Hence,
genes should be identified in the future which would be later tar- isolation of self-flocculating strains and robust bio-flocculation
geted to engineer the selected microalgal strains to achieving would be required to develop in the future.
Strain development: unlike Saccharomyces cerevisiae and marine bacterial–microalgae consortia in a fixed-bed photobioreactor. J.
Hazard. Mater. 292, 155–163.
Escherichia coli, the metabolic engineering systems are not fully
Barnharst, T., Rajendran, A., Hu, B., 2018. Bioremediation of synthetic intensive
established to develop engineered robust algal strains. Hence, it aquaculture wastewater by a novel feed-grade composite biofilm. Int.
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into products is tedious and expensive. It would be better if a Implication of highly metal-resistant microalgal-bacterial co-cultures for the
treatment of simulated metal-loaded wastewaters. Int. Microbiol. 22, 41–
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would be required to conduct detailed studies to elucidate the Benítez, M.B., Champagne, P., Ramos, A., Torres, A.F., Ochoa-Herrera, V., 2019.
technical and economical impact of using residual algal biomass Wastewater treatment for nutrient removal with Ecuadorian native microalgae.
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Byrd, S.M., Burkholder, J.M., 2017. Environmental stressors and lipid production in
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The authors declare that they have no known competing finan- Mar. Biol. Ecol. 487, 33–44.
cial interests or personal relationships that could have appeared Cakmak, T., Angun, P., Demiray, Y.E., Ozkan, A.D., Elibol, Z., Tekinay, T., 2012.
Differential effects of nitrogen and sulfur deprivation on growth and biodiesel
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