Emerging Technology

Received: 19 September 2020 Revised: 24 October 2020 Accepted article published: 2 November 2020 Published online in Wiley Online Library: 19 November 2020

(wileyonlinelibrary.com) DOI 10.1002/jctb.6602

Emerging technologies of algae-based

wastewater remediation for bio-fertilizer
production: a promising pathway to
sustainable agriculture
Yao Zou,a Qingqing Zeng,b Huankai Li,b Hui Liub,c* and Qian Lud*

Abstract
Soil degradation, overuse of chemical fertilizer, and biodiversity loss are serious problems challenging the sustainable devel-
opment of modern agriculture. In recent years, owing to the advantages of algae biotechnology in nutrients recovery and soil
improvement, the integration of algae-based wastewater remediation and algal bio-fertilizer production is emerging into the
limelight. In this work, we emphasize on the progresses achieved in the fields of biomass production by algae cultivation in
wastewater and application of algal bio-fertilizers. Particularly, three types of algal bio-fertilizers, including slow-release bio-
fertilizer, nitrogen-fixing cyanobacteria, and liquid bio-fertilizer, widely evaluated and utilized in agriculture are introduced.
To prevent the overly optimistic prediction of algal bio-fertilizer in a real-world application, we point out the challenges and
technical defects, such as presence of new pollution factors in wastewater, high cost of algal biomass, contamination of algal
biomass in wastewater, low productivity of algae and valuable components, high water consumption, and potential threats
of cyanobacteria to the environment, that prevent the concept of integrating algae-based wastewater remediation and algal
bio-fertilizer production from becoming a reality. Based on our knowledge and experience, potential solutions to the aforemen-
tioned problems are discussed in depth. It is expected that the emerging technologies of algae-based wastewater remediation
for bio-fertilizer production will bring human beings into a new era of environmentally-friendly, high-yield, and resource-
recycling agriculture.
© 2020 Society of Chemical Industry (SCI)

Supporting information may be found in the online version of this article.

Keywords: algae; cyanobacteria; bio-fertilizer; wastewater remediation; nutrients recovery

INTRODUCTION Three algal species, including Chlorella minutissima, Scendesmus

The development of eco-friendly agriculture, in which the environ- sp., and Nostoc muscorum, were grown in sewage wastewater
mental pollutions and ecological disasters are controlled effec- for nutrients removal and biomass synthesis, and value-added
tively, is a goal more and more people in the world share.1 biomass was harvested to produce bio-fertilizer.12 The study by
However, environmental and ecological problems, including the Khan et al. confirmed the practical feasibility of growing algae in
decrease of soil fertility, biodiversity loss, and contamination of wastewater to produce value-added bio-fertilizer. In addition to
underground water, are caused by the overuse of chemical fertil-
izers.2,3 As a category of organic fertilizer made from eukaryotic * Correspondence to: H Liu, Innovative Institute of Animal Healthy Breeding,
microalgae or prokaryotic cyanobacteria, algal fertilizer, which Department of Environmental Science and Engineering, Zhongkai University of
can capture carbon dioxide (CO2), fix nitrogen, and improve soil fer- Agriculture and Engineering, Guangzhou, 510225, China, E‐mail: liuhui@zhku.
tility, is emerging into the limelight.4,5 In addition, since algae are edu.cn; or Q Lu, School of Resources, Environmental & Chemical Engineering,
Nanchang University, Nanchang, 330031, China. E‐mail: [email protected]
able to recover nutrients from wastewater, algae cultivation could
also be employed for wastewater remediation.6,7 Therefore, a novel a Guangdong Society of Environmental Sciences, Guangzhou, China
concept of integrating wastewater-based algae culture with the
exploitation of biomass as bio-fertilizer has been proposed and b School of Resources and Environment, Zhongkai University of Agriculture and
Engineering, Guangzhou, China
studied as an emerging technology for eco-friendly agriculture.8,9
Current studies in this field cover algae-based wastewater reme- c Innovative Institute of Animal Healthy Breeding, Department of Environmental
diation, bio-fertilizer processing, soil ecosystem protection, plants Science and Engineering, Zhongkai University of Agriculture and Engineering,
or crops growth, and food safety chain.5,10,11 For example, Khan Guangzhou, China
et al. proposed the concept of integrating wastewater-based d School of Resources, Environmental & Chemical Engineering, Nanchang Uni-
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algae culture with the exploitation of biomass as bio-fertilizer. versity, Nanchang, China

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the research by Khan et al., many other studies have explored the cultivation could be integrated with wastewater remediation for
effects of algal bio-fertilizer on the microbial community in soil the biomass production. In this model, algae serve as an ‘interme-
ecosystems and the contributions of algal bio-fertilizer to nitro- diate carrier’ to transport the wastewater nutrients to agricultural
gen fixation, providing a deep understanding of the positive roles soil, bringing environmental benefit and economic benefit.
of algal bio-fertilizer in eco-friendly agriculture.13,14 Generally, nutrients removal and biomass composition are two
The algae-based wastewater remediation for bio-fertilizer pro- important concerns in the algae-based wastewater remediation
duction shows the following advantages: (i) Wastewater could for bio-fertilizer production.
be obtained at very low cost, reducing the selling prices of algal
bio-fertilizer; (ii) The algae-based wastewater remediation could Nutrients removal
convert waste nutrients into value-added biomass, creating eco- High removal efficiency of nutrients is expected in the algae-
nomic benefits; 15 (iii) With the nutrients recovery by algae based wastewater remediation to ensure that the effluent can
growth, potential pollution of the wastewater can be dramatically meet the requirements of current regulations. Up to now, it has
reduced;16 and (iv) Harvested biomass can be exploited as algal been proven that a variety of agriculture-related wastewater, such
bio-fertilizer for eco-friendly agriculture. Owing to the great as animal manure, food processing effluent, aquaculture waste-
advantages in the economic and environmental aspects, the pro- water, can be treated by the algae.7,19,20 As shown in Table 1,
duction and application of algal bio-fertilizer is becoming an algae, including microalgae and cyanobacteria, could effectively
emerging technology that is attracting the attention of remove a portion of nutrients in wastewater, and at the same
researchers in both academia and industry. time, produce biomass. In addition, compared with municipal
Up to now, however, this emerging technology has not been wastewater and industrial effluent, agriculture-related wastewa-
widely used in agriculture. To our knowledge, some problems ter contains no or much fewer toxic compounds and are more
(such as high cost of algal bio-fertilizer, contamination of algal bio- likely to be easily obtained in rural areas. Therefore, agriculture-
mass, low productivity of algae and valuable components, high related wastewater can be a good medium to cultivate algae for
water consumption and water loss, and potential threats of cya- bio-fertilizer production.
nobacteria to environment) are challenging the widespread appli- However, it is noteworthy that in some cases the removal effi-
cation of algal bio-fertilizer in agriculture worldwide.17,18 In the ciency of nutrients in wastewater is low (Table 1). As a result, the
foreseeable future, to promote the use of algal bio-fertilizer in discharge of wastewater after algae cultivation will not only cause
agriculture, the aforementioned problems should be fully environmental pollution, but also waste the nutrients in wastewa-
addressed. ter. Previous studies discovered that the low removal efficiency of
In this paper, the application of algae biotechnology for waste- nutrients is partly attributed to the unbalanced nutrients profile
water remediation and bio-fertilizer production is reviewed, and and the suspended organics in wastewater. To overcome this
some emerging breakthroughs in this field are introduced. We problem, a couple of novel solutions have been proposed and
would like to highly commend researchers on their meaningful applied in practice. Firstly, wastewater from different sources
studies related with algal bio-fertilizers and, at the same time, dis- could be mixed to balance the nutrients profile. For example, Leite
cuss the problems challenging the use of algal bio-fertilizers in et al. mixed municipal effluent and piggery wastewater to
agricultural practice. By the end of this work, the prospects of the increase the nutrient concentration for microalgae cultivation.21
production and application of algal bio-fertilizers are discussed. This strategy could effectively improve the biomass yield and pro-
mote the removal of carbon and phosphorus (Table 1). Secondly,
chemical oxidation can be employed to pretreat the wastewater,
TECHNOLOGIES FOR THE PRODUCTION converting suspended organics into dissolved nutrients for algae
AND APPLICATION OF ALGAL growth. The chemical oxidation methods applied in the wastewa-
ter pretreatment process include the Fenton-iron oxidation, hypo-
BIO-FERTILIZER chlorite oxidation, and so forth.7,22 Thirdly, the co-culture of algae
Current studies associated with algal bio-fertilizers can be classi- with bacteria or yeast in wastewater could also be employed to
fied into two important categories. Firstly, a portion of studies promote the nutrients recovery.23 On one hand, bacteria or yeast
explored the algae-based nutrients recovery from wastewater could degrade the suspended organics into low-molecular-
for bio-fertilizer production. This novel technology is regarded weight organics, which are more likely to be assimilated by algal
as a feasible way to reduce the total cost of algal bio-fertilizer cells. On the other hand, algal photosynthesis could provide oxy-
and alleviate the environmental pollution caused by wastewater gen to the bacteria or yeast performing heterotrophic metabo-
discharge. Particularly, the conversion of waste resources into lisms. Such a symbiotic relationship could not only promote the
value-added bio-fertilizer will promote the development of a cir- nutrients recovery, but also improve the biomass yield.
cular economy in the agricultural industry. Secondly, a number
of algal bio-fertilizer products were designed and evaluated in Biomass composition
the agricultural practices. Up to now, three types of algal bio- The fertilization effect of algal bio-fertilizer is partly attributed to
fertilizer (including liquid bio-fertilizer, slow-release bio-fertilizer, the biomass composition. To our knowledge, owing to the impor-
and nitrogen-fixing cyanobacteria) made of algal biomass or liv- tance of the nitrogen element to plant growth, nitrogen-rich bio-
ing algal cells have been developed. mass is regarded as a good feedstock for algal bio-fertilizer
production. Nitrogen in wastewater is important to the nitrogen
Algae-based wastewater remediation accumulation and protein synthesis in algal biomass, but ammo-
To produce affordable bio-fertilizer, wastewater enriched with nia toxicity may limit the algae growth or even cause the failure
nutrients can be employed for algae cultivation. Compared with of algae cultivation. For example, in the study by Lu et al., when
the artificial medium, wastewater could be obtained at low cost, the concentration of ammonia reached 28.03 mM, the growth of
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thus reducing the total cost of algal biomass. Hence, the algae Chlorella sp. in aqueous phase was inhibited.24

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Table 1. Algae-based nutrients recovery from agriculture-related wastewater

Nutrients removal efficiency (%)

Wastewater Algal strain COD TN TP Biomass yield (g L−1) Reference

Meat processing wastewater Chlorella sp. 29.53–43.91% 49.48–50.94% 44.95–54.45% 1.40–1.54 58

Brewery wastewater Leptolyngbya sp. 91.6% 89.4% 98.5% 0.74 6
Meat processing wastewater Scendesmus sp. and Chlorella sp. 72–82% 75–80% 86–92% NAa 7
Fish rearing wastewater Chlorella vulgaris 75.48% 76.56% 92.72% 1.31 79
Agricultural runoff Cyanobacteria NA 95% 99% NA 80
Aquaculture effluent Chlorella vulgaris NA 78.7% 94% 1.39 81
Dairy processing wastewaterChlorella vulgaris 16.44–46.51% 42.58–64.98% 21.79–64.15% NA 67
Agricultural runoff Anabaena sphaerica & Anabaena 77.0–84.2% ~90% ~50% ~1.1 82
variabilis
Swine wastewater Tribonema sp. 49.7–55.6% 80.2–9.9% 66.4–72.7% ~1.4 83
Swine wastewater Synechocystis sp. 62.7–68.6% 73.7–75.8% 71.4–71.6% ~1.6
Rural wastewater Chlorella vulgaris 69.17–88.78% 62.04–82.49% NA 1.34 84
Fish rearing wastewater Chlorella sorokiniana 71.88% 75.56–84.51% 73.35% 1.15–4.02 85
Aquaculture effluent medium Monoraphidium sp. & Scenedesmus sp. NA 82–98% 66–90% 0.6–1.2 20
Hog manure Chlorella vulgaris 95.67% 69.55% 64.40% 7.37 g/m2 86
Digested dairy manure Chlorella sp. 27.4–38.4% 75.7–82.5% 62.5–74.7% 1.47–1.71 87
Cattle manure Scenedesmus sp. Over 90% Over 90% 79–88% 2–4 19
a
‘NA’ refers to ‘not available’.

To alleviate the ammonia toxicity in wastewater, previous stud- Slow-release bio-fertilizer

ies employed a variety of pretreatment methods.25,26 For exam- According to previous studies, the algae that can be cultivated as
ple, the pretreatment by nitrification and ammonia stripping the feedstock of slow-release bio-fertilizer include Nannochlorop-
could reduce the concentration of ammonia in wastewater via sis sp., Chlorella sp. and Spirulina sp., among others.28,30 Most of
nitrifying bacteria activity and air bubbling, respectively, thus cre- the algae exploited for slow-release bio-fertilizer have a high con-
ating a favorable environment for algae growth. In addition, Lu tent of protein, from which the degradation in soil can release a
et al. reported the feasibility of using zeolite to absorb ammonia large amount of nitrogen.28 The processes of biomass degrada-
at the initial stage and then release ammonia into wastewater at tion and nutrients release are catalyzed by the microorganisms
the later stage for the growth of Spirulina sp.25 The addition of in soil. It was reported that Proteobacteria (35–42%), Acidobacteria
zeolite in wastewater could not only alleviate the ammonia toxic- (12–15%), and Bacteroidetes (8–10%) became the most abundant
ity, but also mitigate the nitrogen deficiency at the later stage of microbial species in the cucumber rhizosphere when algal bio-
algae cultivation. Owing to the continuous supply of nitrogen by fertilizer was added in the soil.31 The biomass degradation cata-
zeolite, algae with high protein content (69.8% of total dry lyzed by the microbial activities is a slow process, increasing the
weight) and high biomass yield (4.31 g L−1) were obtained.25 effective duration of algal bio-fertilizer. Besides this, algal biomass,
microorganisms, and inorganic particles can form an adherent
network in soil, reducing the nutrient loss of fertilizer in the pro-
Application of algal bio-fertilizer cess of irrigation.32,33 Therefore, the slow-release algal fertilizer
Current studies cover both fundamental research and applied shows greater advantages over traditional chemical fertilizers.
research, fully documenting the positive effects of algal bio- Normally, the production process of slow-release algal fertilizer
fertilizers on plant growth, crop yield, soil microorganisms, nutri- involves the algae cultivation, biomass dehydration, and biomass
tional value of fruits, and seed germination.9–11 Driven by the eco- pasteurization or pulverization.30 It is noteworthy that the dehy-
logical and economic benefits, researchers from academia and dration process is meant to lower the moisture content in algal
industry have developed three major models to utilize the algal biomass and prevent the excessive deterioration of bio-fertilizer
bio-fertilizers in agriculture (Fig. 1). Firstly, algal biomass, which during storage. In some cases, this process, together with algae
can be degraded by the soil microorganisms, serves as a slow- cultivation and biomass harvesting, might be highly energy-
release fertilizer to continuously provide nutrients to plants.27,28 intensive, resulting in the high cost of algal bio-fertilizer. In the
Secondly, living algal cells could be added into soil to regulate study by Lv et al., microalgae biomass was suspended in tap water
the microbial community, improve soil fertility, and control soil as bio-fertilizer to support the growth of cucumber without dehy-
moisture.14,29 Thirdly, algae extract containing amino acids and dration or pasteurization.31 In this way, the energy consumption
minerals can be exploited as a liquid bio-fertilizer that is spread and total cost of the algal bio-fertilizer can be dramatically
on the surface of plant leaves.10 Although slow-release bio-fertil- reduced. In addition, Rothlisberger-Lewis et al. used lipid-
izer, nitrogen-fixing cyanobacteria, and liquid bio-fertilizer are dif- extracted algae as the feedstock of bio-fertilizer, thus ensuring
ferent in their production processes and action mechanisms, all of the integration of biodiesel production and bio-fertilizer produc-
them can have positive effects on plant growth and soil quality tion.34 The aforementioned novel technologies can be regarded
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(Table 2). as important attempts to produce affordable algal bio-fertilizer.

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Figure 1. Three models of utilizing algal bio-fertilizers in agriculture.

The important roles of slow-release algal fertilizer in agriculture provide nitrogen to agricultural crops, but also improve the soil
mainly include the support of plant growth and the improvement quality and protect the plants or crops.5,36
of soil quality. Firstly, the nutrients, such as nitrogen, phosphorus, The use of nitrogen-fixing cyanobacteria in agriculture shows
organic carbon, and minerals, released from algal fertilizer can be advantages in five aspects. Firstly, with the metabolisms of
assimilated by plants. Coppens et al. reported that, in the growth nitrogen-fixing cyanobacteria, nitrogen in the atmosphere can
of tomatoes, the addition of algal bio-fertilizer not only increased be transported into the soil to support plant growth. It was
the leaf length and leaf fresh weight, but also promoted the accu- reported that cyanobacteria fertilizer could add up to 20–30 kg
mulation of glucose, fructose, and carotenoids in tomato fruits.30 nitrogen ha−1 to agricultural crops.5,36 Thus, the application
The positive effects of algal bio-fertilizers on plant growth have amount of chemical nitrogen fertilizer in agriculture can be low-
also been reported in many other studies (Table 2). Secondly, ered. Secondly, cyanobacteria could release extracellular poly-
the nutrients released from algal fertilizer could improve the soil meric substances and plant growth-promoting (PGP)
fertility. It has been reported that algal bio-fertilizer increased substances, which can improve the soil quality and support plant
the contents of available nitrogen, phosphorus, and potassium growth, respectively.37 Specific contributions of nitrogen-fixing
in soil, therefore providing the plants with more sufficient nutri- cyanobacteria to soil quality improvement and plant growth are
ents.27 Also, at the harvest stage, the contents of nitrogen, phos- presented in Table 2. Thirdly, some cyanobacteria could lower
phorus, and potassium that remained in the soil fertilized by the incidence rate of agricultural diseases. Previous studies
algal biomass were higher than the contents of nutrients in other reported that cyanobacteria could limit the growth or invasion
experimental groups. Hence, the use of algal bio-fertilizer could of pathogenic microorganisms, such as Fusarium wilt, Rhizoctonia
protect the soil quality for a long period of time. solani, Sclerotinia sclerotiorum, and Alternaria porri.38,39 Fourthly,
cyanobacteria could support the formation of biological soil crust,
which plays a key role in the prevention of land desertification.
Nitrogen-fixing cyanobacteria Tiwari et al. discovered that exopolysaccharides (EPSs) secreted
The nitrogen-fixing cyanobacteria refer to a category of blue- by nitrogen-fixing cyanobacteria mainly contributed to the con-
green algae that can absorb nitrogen directly from the air. To solidated structure of soil crust, thus retaining the humidity in soil
our knowledge, not all blue-green algae have the ability of assim- and improving the water availability.40 Last but not least, since
ilating nitrogen in air and the nitrogen-fixing cyanobacteria algae can be regarded as a huge carbon sink, the living cyanobac-
mainly include the genera Nostoc and Anabaena.35 The living cya- teria in soil will partly compensate for the carbon dioxide (CO2)
554

nobacteria used as bio-fertilizer could not only continuously emissions of agriculture.41 Therefore, the wide application of

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Table 2. Effects of algal bio-fertilizer on plant growth and soil quality

Algal bio-
fertilizer Algal species Pant or crop Parameters Main conclusion Reference

Slow-release Chlorella sp., Corn plant Plant: dry weight, metal (Fe, Zn, Mn The use of digested Chlorella sp. at 88
bio- Neochloris & Cu) content, uptake of macro- 5 t ha−1 promotes plant growth
fertilizer conjuncta & elements (N, P, K, Ca, & Mg) and increases the contents of
Botryococcus metals in corn plant.
braunii
Acutodesmus Roma tomato Plant: numbers of lateral root, Algal fertilizer enhances plant 89
dimorphus plant flower bud, and branch; total growth and floral production.
fresh plant weight
Nannochloropsis Tomato plant Plant: leaf length and weight, metal (1) With regard to plant growth, 30
oculata and fruit (K, Ca, Mg, Zn, Mn, Fe, & Cu) algal biomass can replace
content conventional fertilizer. (2) Algal
Fruit: fruit yield, contents of sugars fertilizer improves fruit quality
and carotenoids by increasing the contents of
sugars and carotenoids in
tomato fruits.
Chlorella sp. Corn seed and Seed: germination rate and (1) Algal bio-fertilizer increases the 90
plant germination period germination rate of seeds and
Plant: length of roots and leaves, shortens germination period. (2)
weight of roots and leaves, Algal fertilizer promotes the
photosynthesis activity growth of roots and leaves and
enhances photosynthesis.
Chlorella vulgaris Wheat Plant Plant: weights of shoot and root, Algal biomass is a viable option for 91
root density, length, and delivering nutrients to support
diameter; agriculture on marginal soils.
Chlorella vulgaris Rice plant Plant: plant height, number of (1) Chlorella vulgaris and Spirulina 28
& Spirulina leaves per plant, plant weight, platensis can be used as bio-
platensis leaves area per plant, seed yield fertilizer to enhance rice yield.
characters (2) Algal bio-fertilizer improves
Soil: soil biological activity (CO2 the biological and chemical
evolution, dehydrogenase properties of the soil.
activity, nitrogenase activity,
etc.), soil chemical properties
(pH, available-N, available-P,
available-K)
Tetraselmis sp. Date palm Plant: numbers of roots and leaves, The addition of appropriate 27
shoot length, stem thickness amount of algal biomass in soil
chlorophyll concentration promotes plant growth,
Soil: total N, total P, total K improves the elemental
composition of soil and
maintains a safe low level of
heavy metals in soil.
Nannochloropsis NAa Soil: content of organic carbon, (1) Algal biomass after lipid 34
salina microbial biomass carbon, total extraction can be used as a soil
N, extractable inorganic N, etc. amendment for agricultural
production. (2) At high addition
rates, problems with excess soil
salinity and sodicity may occur.
Chlorella vulgaris Wheat plant Soil: P content in soil (1) P release from algal biomass 92
increases the concentrations of
labile and moderately labile P
fractions in soil. (2) Algal
fertilizer releases P when
incorporated into the soil to
support or even sustain plant
nutrition
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Table 2. Continued

Algal bio-
fertilizer Algal species Pant or crop Parameters Main conclusion Reference

Cyanobacteria Nostoc muscorum NA Soil: activities of enzymes Cyanobacterial biomass and 93

& Tolypothrix (⊎-glucosidase, urease, exopolysaccharide result in an
tenuis arylsulphatase, protease, etc.) increase of enzymatic activities
Anabaena Common bean Plant: plant height, number of Bio-fertilizer increases nodulation, 94
cylindrica nodules, nodule dry matter, plant growth, and production of
shoot dry matter, accumulated the common bean.
shoot nitrogen, number of pods
per plant, number of grains per
pod, hundred grain weight, grain
plant weight
Consortia of Pearl millet & Soil: nutrient dynamics in soil, (1) Cyanobacteria perform well in 95
Nostoc wheat microbial activities, physical bioameliorating salt-affected
ellipsosporum characteristics (bulk density, semi-arid soils. (2) Grain yield
and Nostoc water holding capacity, etc.) and leaf area are improved.
punctiforme Plant: leaf area, spike length, grain
yield, protein content
Nostoc sp. and NA Soil: formation of soil surface Cyanobacteria promote the 13
Anabaena sp. consortia, biomass adherence to formation of soil surface
soil under water flush treatment consortia and improve surface
stabilization of agricultural soil
Oscillatoria sp., NA Soil: soil microbiota, contents of Cyanobacteria improve crust 14
Nostoc sp. and available nutrients (P, K, Na, Ca & formation, favor the
Scytonema sp. Mg) proliferation of other
microorganisms, and restore
microbial populations in soil
Leptolyngbya sp., NA Soil: soil physicochemical (1) Cyanobacteria are able to 29
Oscillatoria sp., properties and soil stability colonize soils from arid and
Microcoleus parameters semi-arid areas. (2) Extracellular
vaginatus, polymeric substances secreted
Nostoc by cyanobacteria blind soil
commune, etc. particle together, increasing
surface stability and reducing
clay dispersion.
Nostoc carneum, Chamomile Plant: weights of shoot and root, (1) Cyanobacteria promote the 96
Wollea lengths of shoot and root, flower plant growth and increase the
vaginicola, & head diameter and weight, weight of essential oil. (2) Wollea
Nostoc weight of essential oil vaginicola dramatically
punctiforme Soil: contents of nutrients (Ca, P, & increases the P content in soil
N)
Nostoc sp. & NA Soil: biological soil crust quality Inoculation of cyanobacteria lead 32
Oscilatoria sp. indicators, soil loss to the biological soil crust
formation and prevent the soil
loss
Liquid bio- Liquid extract of Tomato plant Plant: root length, root weight, Liquid extracts of algae stimulate 97
fertilizer cyanobacteria, shoot length, shoot weight, root plant growth, enhance nutrient
Chlorophyta, concentrations of N, P and K uptake, and change metabolite
Rhodophyta, profile of tomato
etc.
Acutodesmus Tomato seed Seed: germination rate Algal extract triggers faster seed 89
dimorphus and plant Plant: numbers of lateral root, germination and results in
extract flower bud, and branch; total greater numbers of flowers and
fresh plant weight branches per plant
Chlorella Wheat plant Plant: lengths of roots and shoots, Algal extract increases lengths of 98
sorokiniana fresh weights, and dry weights roots and shoots, fresh weights,
suspension and dry weights of wheat plant
556

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Table 2. Continued

Algal bio-
fertilizer Algal species Pant or crop Parameters Main conclusion Reference

Marine Carrot cell (seed) Seed: germination rate Algal extract increases the 99
cyanobacterial germination rate of artificial
extract seeds
(Synechococcus
sp.)
Microcystis Willow plant Plant: height, fresh mass, number Foliar application of algal fertilizer 100
aeruginosa, of shoots per plant, index of promotes plant growth and
Anabaena sp., chlorophyll content in leaves, biomass yield and increases
and Chlorella activity of RNase and total chlorophyll content in leaves
sp. dehydrogenases and photosynthetic rate
Chorococcum sp. Vigna radiata, Plant: numbers of leaves and roots, (1) A maximum growth rate is 10
extract Solanum lengths of root and shoot, found in 20% algal liquid
lycopersicum, biochemical parameters (total fertilizer. (2) Algal liquid fertilizer
Cucumis protein, lipid, carbohydrate, at higher concentration inhibits
sativus & phenol), contents of pigments the growth and results in lower
Capsicum (total chlorophyll and biochemical content.
annuum carotenoids)
a
‘NA’ refers to ‘not available’.

nitrogen-fixing cyanobacteria can be a promising pathway to sus- noteworthy that some physical methods have high energy con-
tainable agriculture. sumption and require special equipment. (ii) Enzymatic degrada-
In the practice, cyanobacteria can be applied in the forms of micro- tion refers to the method of adding cellulase, mannanase,
bial inoculant and microbial biofilm.42 Firstly, it is the most straight- xylanase, or pectinase to degrade certain compounds in cell
forward way to add cyanobacteria cells into soil as microbial walls.44,45 Compared with the physical methods and chemical
inoculant. Previous studies discovered that cyanobacteria could methods, enzymatic degradation can be conducted in a much
improve the soil quality and promote plant growth (Table 2). Never- milder environment, alleviating the damage of cell wall breakage
theless, in some cases, microbial inoculants may suffer from the to the value-added biomass compositions.44 Some parameters,
problem of poor survival in soil, and their PGP abilities are depen- such as pH, incubation time, temperature, and enzyme concentra-
dent upon their competence in this niche.42 Secondly, the cyano- tion, should be optimized to improve the performance of enzy-
bacteria biofilm can be prepared before the inoculation of matic degradation in the breakage of cell walls. In some cases,
microorganisms in soil. In a real-world application, to improve the to improve the treatment efficiency, some of the aforementioned
performance of biofilm in soil protection, cyanobacteria can be methods can be combined for the breakage of algal cell walls.
mixed with other microorganisms in the preparation of biofilm.42 As shown in Table 2, liquid bio-fertilizer could effectively pro-
mote the growth of plants or crops. For example, Vijayakumar
Liquid bio-fertilizer et al. discovered that the liquid bio-fertilizer provided amino acids
Liquid bio-fertilizers mainly refer to the algal extracts enriched and essential minerals to Capsicum annum, improving the root
with the nutrients essential to plant growth (Table 2). In the foliar length, total dry weight, leaf area, and the number of branches
application of algal extracts, nutrients could enter the plants or and pods.11 The positive effects of algal bio-fertilizers on the
crops via leaf pores. Compared with the slow-release fertilizer, growth of other plants or crops, such as Vigna radiata, Cucumis
the liquid bio-fertilizer can be utilized by plants and crops in a sativus, and Oryza sativa, were also reported.10,46 Therefore, the
more efficient way. Also, with the widespread application of liquid algal bio-fertilizer industry is of vital importance to agricultural
bio-fertilizer in agriculture, the problems caused by the traditional development.
fertilizers, such as fast growth of weeds after fertilization, nutrients
uptake being restricted by low temperature, and nutrients loss
after irrigation, can be alleviated effectively. Hence, the use of liq- CHALLENGES AND TECHNICAL DEFECTS
uid bio-fertilizer made from algal biomass is becoming an emerg- Although previous studies optimized the cultivation conditions
ing trend in eco-friendly agriculture. for microalgae-based wastewater remediation and explored the
To produce the liquid bio-fertilizer, an essential step is to break positive effects of algal bio-fertilizers on ecosystem and agricul-
the cell wall of algae in a cost-saving and efficient way. Up to now, ture, there are a few problems challenging the emerging technol-
the methods that can be applied to break the cell wall include ogy of algae-based wastewater remediation for bio-fertilizer
high pressure gases treatment, bead milling, ultrasound treat- production (Fig. 2).
ment, alkaline digestion, enzymatic degradation, and so on:
(i) High pressure gases treatment, bead milling, and ultrasound Presence of new pollution factors in wastewater
treatment belong to the physical methods, which break the struc- It has been widely documented that algae could remove the
557

ture of algal cells by physical impacts or shocks.43 However, it is nutrients, such as nitrogen, phosphorus, and organic carbon, in

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Figure 2. Technical defects of algae-based wastewater remediation for bio-fertilizer production.

wastewater.7,47 However, this does not mean that algae culture is culture, algae harvesting, biomass dehydration, and fertilizer
a perfect technology for wastewater remediation, since new pol- preparation, making the costs of biomass and algal bio-fertilizer
lution factors may be introduced into the aqueous phase. Firstly, remarkably high50 It was reported that in current microalgae pro-
algae growth could increase the pH value of wastewater and alka- duction systems, the biomass production cost ranges between
line wastewater is not allowed to be directly discharged. In the 5 €/kg for open raceway pond and 50 €/kg for photo-bioreactor.51
study by Khan et al., the pH value of wastewater reached 9.32 after In the study by Acién et al., the total cost of algal biomass was
algae culture.12 Cardoso et al. demonstrated that the growth of reduced from 69 to 12.6 €/kg by scaling up the production capac-
Spirulina sp., a category of cyanobacteria usually used as feed- ity.50 If the nitrogen content in dry biomass was set to 5.87%, the
stock of bio-fertilizer, even increased the pH of culture medium unit cost of nitrogen element would be over 214.65 €/kg. As a
to 10.60.47 Secondly, a number of prokaryotic cyanobacteria could result, the algal bio-fertilizer, showing no advantages over chem-
release toxic components, causing ecological disasters in water ical fertilizer in the aspect of production cost, would not be afford-
bodies.48 For example, Nostoc muscorum, which was used in the able to farmers.17,52 Owing to the low profitability of traditional
study by Oudra et al., could synthesize microcystins.49 Thirdly, agriculture in developing countries, it is not the best choice for
after wastewater treatment, a portion of living algae may be left farmers to use the algal bio-fertilizer to replace chemical fertilizer
in the aqueous phase since most techniques could not ensure in the large-scale agricultural production.
100% harvesting efficiency. With the discharge of wastewater,
the living cyanobacteria will enter bodies of water, causing algal
Contamination of algal biomass
bloom and disturbing ecological balance.
Some wastewater containing toxic pollutants, particularly heavy
Owing to the new pollution factors brought by algae, particu-
metals, could contaminate the algal biomass, resulting in the
larly cyanobacteria, the roles of algae in wastewater remediation
accumulation of toxic pollutants in soil and crops.53 In addition,
should be comprehensively assessed. In our view, these new pol-
algae, the cell surface of which is enriched with functional groups
lution factors, particularly the cyanobacteria toxins and the alkali-
(such as hydroxyl and carboxyl), are negatively charged, and
zation, might be more threatening to environment than eutrophic
therefore perform well in the adsorption of heavy metals.54,55
wastewater.
Hence, algae culture is a process not only assimilating nutrients
from culture media, but also adsorbing and accumulating heavy
High cost of algal biomass metals.54 Heavy metals could enter algal cells either by means of
High production cost is one of the serious problems hindering the active transport or by endocytosis through chelating proteins.56
industrial application of algal biomass. The process of algal bio- According to the report by Kumar et al., the maximum uptake
558

fertilizer production consists of algae strains screening, algae rates of Cd, Cr, Cu, Hg, and Pb by living algal cells could reach

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105, 304, 576, 15, and 188 mg g−1, respectively.54 As a result, the biomass yields of microalgae and cyanobacteria in autotrophic
algae culture in some wastewater might become a process of model could reach 0.5–4.0 kg m−3, suggesting that around
adsorbing and accumulating heavy metals. With the degradation 1 ton water would be consumed to produce 0.5–4.0 kg algal bio-
of bio-fertilizer in soil, the heavy metals concentrated in algal bio- mass. In addition, since open ponds are usually employed to pro-
mass would be released, resulting in the contamination of farm- duce algae at a large scale, water loss caused by evaporation
land and plants. should be considered. It was reported that the evaporation rates
Continuous use of wastewater for irrigation could result in the of lakes in tropical and temperate zone could reach 5.1 and
accumulation of heavy metals in soil and eventually lead to 3.1 mm day−1, respectively.59,60 In other words, during a 10-day
increased uptake of heavy metals by crops and plants.57 Hence, culture period, about 3.1–5.1 m3 water will be lost by evaporation
the soil irrigation by wastewater, which can cause serious ecolog- in a 100 m2 open pond for algae production. Thus, the high water
ical disasters and environmental pollutions, is strictly prohibited in consumption and water loss of algae culture may cause serious
many countries. In our view, if heavy metals in wastewater are not environmental problems or ecological disasters if algal bio-
treated properly, the use of algal bio-fertilizer for soil fertilization fertilizers are widely produced and used in arid or semi-arid
will be another form of irrigating farmland by using wastewater, countries.
since algal bio-fertilizer could transport a portion of toxic pollut-
ants into soil.
Potential threats of cyanobacteria to environment
Low productivity of algae and valuable components Living cyanobacteria are added into soil as bio-fertilizer to fix
To meet the requirements of plant growth, nitrogen and phos- atmospheric nitrogen and convert it into an available forms
phorus should be provided continuously through fertilization. at no cost to plant growth, but the potential threats, such as
However, the productivity of nitrogen and phosphorus in algae cyanobacteria toxin and biological invasion, are neglected.61–63
culture are too low to support the wide application of algal bio-fer- 63 Firstly, some cyanobacteria could release toxins, such as
tilizer. In the study of Khan et al., the period of phytoremediation microcystins, nodularins, aplysiatoxins, cylindrospermopsin, sax-
and algae culture were set as 25-day, but the biomass yields of itoxins, anatoxin, and lyngbyatoxin, which might contaminate
algae were only 0.14–0.45 g L−1.12 If the maximum contents of the soil or even the underground water.64 It was even observed
nitrogen and phosphorus in algal biomass were set as 5.87% that microcystins were accumulated in salad lettuce and clover,
and 0.95%, respectively,12 the productivity of nitrogen and phos- threatening the safety of food chains.65,66 Secondly, living cya-
phorus in algae grown in sewage wastewater were only 0.329–- nobacteria used as bio-fertilizers may migrate to the water bod-
1.057 g −1m−3 day−1 and 0.053–0.171 g−1 m−3 day−1. If these ies near farmland, resulting in algal bloom and biological
data are applicable in industry, to produce bio-fertilizer with invasion.61 This problem is remarkably threatening to the farm
1 ton nitrogen per day, 9.464 × 105–3.042 × 106 m3 sewage ecosystem of modern agriculture, which usually integrates crop
wastewater and 1.89–6.08 km2 areas would be needed (Table 3). planting and fish culturing.
During the year of 2019, 3.696 × 107 ton nitrogen fertilizer was In addition to the aforementioned problems, some other unfa-
produced in China to meet the demand of agriculture. In this case, vorable factors, such as the residual nutrients in wastewater after
to replace the chemical nitrogen fertilizer with algal bio-fertilizer, algae cultivation, inconvenience in the transportation and storage
1.914 × 105–6.157 × 105 km2 areas, accounting for 2.00–6.41% of of liquid bio-fertilizer, uncontrolled degradation rate of algal bio-
all the land of China (9.6 × 106 km2), will be needed for algae cul- mass used as slow-release bio-fertilizer, and low consumer-
ture. In a real-world application, it is not feasible to use such a acceptance of bio-fertilizers, are hindering the application of algal
huge land area for the production of algal bio-fertilizer. Therefore, bio-fertilizer in agriculture worldwide.
owing to the low productivity of algae and valuable components,
the total production capacity of algal bio-fertilizer will be very lim-
ited, further hindering the widespread use of bio-fertilizer in POTENTIAL SOLUTIONS AND PROSPECTS
agriculture. The presentation of problems challenging the production and
application of algal bio-fertilizer is not to deny its importance
Water consumption and water loss and promising prospects. According to our judgment, some tech-
Algae production is a water-consuming process that requires the nical improvements, novel concepts, and policy support can be
input of a large volume of water and generates wastewater con- good solutions to the aforementioned problems and support
taining residual nutrients or other polluting agents.58 Normally, the wide use of algal bio-fertilizer.

Table 3. Calculation parameters of algal biomass production in wastewater

Nitrogen (N) Phosphorus (P)

Maximum percentage (%) 5.87 0.95

Productivity (g/m3/day) Maximum Minimum Maximum Minimum
1.057 0.329 0.171 0.053
Volume of wastewater (m3) 9.464 × 105 3.042 × 106 5.848 × 106 1.880 × 107
Area of algae culture systema(m2) 1.893 × 106 6.084 × 106 11.696 × 106 37.594 × 106
Area of algae culture systema(km2) 1.893 6.084 11.696 37.594
a
Open raceway ponds with 0.5 m depth are applied for algae culture and wastewater remediation.
559

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Nutrients recovery from wastewater with a high level of Utilization of non-toxic microorganisms
safety Non-toxic microorganisms can be utilized to prevent the potential
Wastewater-based algae growth is a promising way to reduce the threats of cyanobacteria toxins to ecosystem. To our knowledge,
biomass production cost, but only wastewater with a high level of some microorganisms, including Rhodospirillum rubrum, Bacillus
safety should be used to obtain the pollutant-free biomass. To our pumilus, and Bacillus subtilis, perform well in nitrogen fixation
knowledge, food processing effluent, slaughterhouse effluent, and have no toxic effects on plants and ecosystem.73–75 Besides,
and straw fermentation wastewater without toxic components Bacillus sp., which are widely spread in atmosphere, farmland,
could be regarded as wastewater with a high level of safety.67,68 and water, will not cause biological invasion even if they enter
In addition, the wastewater from food or feed industries can be into the soil and water via wastewater or irrigation water. Previous
easily obtained at no cost in rural areas. Thus, the use of ‘highly- studies widely documented the use of these non-toxic microor-
safe’ wastewater from food or feed industries to grow algae and ganisms in farmland management and proved their positive
produce bio-fertilizer will realize resource reutilization in rural effects on plant growth and environmental protection.73,76 Some
areas and support the development of a circular economy. of these non-toxic microorganisms are regarded as probiotics, the
accumulation of which in the food chain will not threaten animal
or human health. In our view, it can be a promising way to allevi-
Desorption of heavy metals on algal cells ate the threats of cyanobacteria toxins to ecosystem by employ-
Heavy metals could be combined with algal cells in the forms of ing non-toxic microorganisms for nitrogen fixation in farmland.
extracellular adsorption and intracellular chelation. Normally, However, one of the challenges to the use of Bacillus sp. as bio-
heavy metals adsorbed on algal cells are more likely to be fertilizer is that the harvesting cost of bacterial biomass is much
removed by desorption treatment, thus reducing the total higher than that of filamentous cyanobacteria. Normally, filamen-
amount of heavy metals in algal biomass. Previous studies have tous cyanobacteria could be efficiently harvested via simple sedi-
discovered that the addition of chelating agents and the pH mentation or filtration, while the thickening process of bacteria is
adjustment are effective methods to promote desorption of time-consuming and energy-intensive.77 Hence, to promote the
heavy metals, and they have studied the desorption kinetics.69 use of beneficial bacteria, such as Bacillus sp., as bio-fertilizer for
Particularly, the desorption treatment methods are affordable nitrogen fixation in soil, the biomass thickening techniques
and will not dramatically increase the total cost of algal bio-fertil- should be improved.
izer. Therefore, it may be a feasible way to prevent the soil con-
tamination caused by the heavy metals in bio-fertilizers by Policy support, government subsidy, and international
conducting appropriate desorption treatment. cooperation
The use of algal bio-fertilizers could effectively minimize green-
house effects, since the algae culture is a carbon-absorbing pro-
Integrated culture of algae and bacteria for water-quality
cess, while the production of chemical fertilizer releases a huge
control
amount of CO2 into the atmosphere.78 Therefore, the benefits
As documented by a previous study, residual nutrients and
brought by algal bio-fertilizer industry to society and natural envi-
increased pH value are the main water-quality problems in the
ronment are numerous. In our view, it is necessary for govern-
wastewater after algae growth.55 The integrated culture of algae
ments to include algal bio-fertilizer industries into the carbon
and bacteria can be a potential solution to the water-quality prob-
trading market and provide a subsidy to reward their contribu-
lems. Firstly, bacteria could degrade the suspended organic solids
tions to environmental protection. With the policy support and
in wastewater to dissolved nutrients available for algae growth. At
government subsidy, the financial burden of algal bio-fertilizer
the same time, oxygen produced by photosynthetic algae could
industries will be relieved and the development of sustainable
support bacterial growth and metabolisms. The algal-bacterial
agriculture will be promoted.
cooperation has been proven to be an effective way for nutrient
International cooperation is also important to the widespread
recovery in wastewater.23 Secondly, some bacteria could convert
use of algal bio-fertilizer. At present, the technologies for the pro-
organics in wastewater into volatile fatty acids, such as acetic acid,
duction and application of algal bio-fertilizer are very novel and
propionic acid, and butyric acid, resulting in the decrease of the challenged by some potential problems or risks. Hence, interna-
pH value of wastewater.70 Thus, the pH increase caused by algae tional cooperation is highly needed to promote the information
growth will be alleviated by the bacterial activities. exchange and support the sustainable development of algal
bio-fertilizer industry.
Water loss control in microalgae cultivation
To overcome the problems of water shortage in arid or semi-arid CONCLUSION
countries, immobilized culture method and closed photo- In conclusion, greater awareness regarding the benefits of algae-
bioreactor are considered possible ways to produce algal biomass based wastewater remediation for bio-fertilizer production is
with low water consumption. Immobilized culture refers to the increasing and there is huge market potential for algal bio-
method of growing microalgae on a substrate or film.71 In some fertilizer industry. In our view, the strategies of converting wasted
cases, the water can be sprayed on the surface of film, thus reduc- resources into algal bio-fertilizer, desorbing heavy metals on algal
ing the water loss caused by evaporation to a lower level. In addi- cells, controlling water loss in algae cultivation, employing
tion, the closed photo-bioreactor, which has a much smaller area non-toxic microorganisms, and proving policy support and gov-
directly exposed to air, may have lower water evaporation than ernment subsidy can partly solve current problems of algal bio-
open raceway ponds.72 In a real-world application, more efforts fertilizer and support the sustainable development of agriculture.
should be devoted into the assessment of water loss and water It is expected that the technical advancement and policy support
560

input of these methods under specific conditions. will bring about an epoch-making breakthrough to the algal

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