“Beyond the Source of Bioenergy”: Microalgae in Modern Agriculture as a Biostimulant, Biofertilizer, and Anti-Abiotic Stress
Abstract
:1. Introduction
Biology of Microalgae
2. Growing Microalgae
2.1. Growth Parameters
2.2. The Biochemical Constituent of Microalgae
2.3. Production Schemes
2.3.1. Open Pond Systems
2.3.2. Racetrack System
2.3.3. Closed System (Photobioreactor)
3. Microalgae-Derived Extracts (Bioactive Compound and High-Value Product)
3.1. Extraction Methods of Microalgae Extract
3.1.1. Novel Techniques of Extraction
Supercritical Fluid Extraction (SFE)
Pressurized Liquid Extraction (PLE)
Microwave-Assisted Extraction (MAE)
Ultrasound-Assisted Extraction (UAE)
Enzyme-Assisted Extraction (EAE)
3.2. Chemical Constituents of Microalgae Extracts
3.3. Application Methods of Microalgae Extracts
4. Microalgae Extracts as Biostimulant and Biofertilizer
5. As Alleviator of Abiotic Stress
6. Future Direction
7. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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ALGAE | Chlorophyll | Other Pigments | Organelle Characteristics | |||||||
---|---|---|---|---|---|---|---|---|---|---|
Taxonomic Class | Size | a | b | c | Bili Protein | Carotenoids | Eukaryote | Mesokaryote | Prokaryote | Storage Product (s) |
Bacillariophyceae | 5–2000 μm | ✓ | - | ✓ | Nil | β-Carotene, Fucoxanthin | ✓ | ✓ | ✓ | Lipids and Chrysolaminarin |
Charophyceae | May exceed 30 cm in length | ✓ | ✓ | - | Nil | β-Carotene, Zeaxanthin, Lutein, Violaxanthin, Neoxanthin | ✓ | ✓ | ✓ | Starch |
Chlorophyceae | 10–80 μm | ✓ | ✓ | - | Phytochrome | Zeaxanthin, Lutein, Violaxanthin, Neoxanthin, Loroxanthin. | ✓ | ✓ | ✓ | Lipids and Starch |
Chrysophyceae | ca. 2 μm–ca. 2 mm | ✓ | - | ✓ | Nil | β-Carotene, fucoxanthin | ✓ | ✓ | ✓ | Lipids and Chrysolaminarin |
Cryptophyceae | 10–50 μm | ✓ | - | ✓ | Phycoerythrin | α-Carotene, Alloxanthin, Crocoxanthin | ✓ | ✓ | ✓ | Starch |
Cyanophyceae | Vary considerably in size | ✓ | - | ✓ | Allophycocyanin, c-Phycocyanin | Flavacene β-Carotene, | - | - | ✓ | Polyphosphate Phycobilins |
Dinophyceae | 50–59 µm | ✓ | - | ✓ | Nil | β-Carotene, Diatoxanthin, Monadoxanthin, Dinoxanthin | - | ✓ | - | Starch (amylose or amylopectin) |
Euglenophyceae | ~35 μm | ✓ | ✓ | - | Nil | β-Carotene, Diatoxanthin, Diadinoxanthin, Monadoxanthin | - | ✓ | - | Paramylon, β-1,3 polymer of glucose |
Haptophyceae | 3–7.5 μm | ✓ | - | ✓ | Nil | β-Carotene, Diatoxanthin, Diadinoxanthin, Fucoxanthin | ✓ | ✓ | ✓ | Water-soluble 1–3 glucan chrysolaminarin |
Phaeophyceae | Range of morphologies and sizes | ✓ | - | ✓ | Nil | β-Carotene, Fucoxanthin, Violaxanthin | ✓ | ✓ | ✓ | Luminaria, Lipids |
Prasinophyceae | ca. 0.95 μm | ✓ | ✓ | - | Nil | β-Carotene, Micronone, Neoxanthin, Zeaxanthin, Lutein, Violaxanthin | ✓ | - | - | Starch |
Rhodophyceae | maximum is ~50 cm | ✓ | - | - | Allophycocyanin, c-Phycocyanin, Phytochrome | β-Carotene, Diatoxanthin, Monadoxanthin, Dinoxanthin | ✓ | ✓ | ✓ | Floridean starch |
Xanthophyceae | ca. 2 μm–ca. 2 mm | ✓ | - | ✓ | Nil | β-Carotene, Diatoxanthin, Diadinoxanthin, Heteroxanthin | ✓ | ✓ | ✓ | Lipids, chrysolaminarin. |
Parameters | Temp °C | Salinity (g L−1) | Light Intensity (mmol m−2 s−1) | Photoperiod (Light: Dark, h) | pH |
---|---|---|---|---|---|
Range | 16–27 | 12.0–40 | 15–135 (depends on volume and density) | NR | 7.0–9.0 |
Optimum | 18–24 | 20–24 | 40–70 | 16:8 (minimum) 24:0 (maximum) | 8.2–8.7 |
Algae | Carbohydrate (%) | Lipid (%) | Protein (%) | References |
---|---|---|---|---|
Arthrospira platensis | 8–20 | 4–9 | 49–65 | [27,34] |
Chlorella species | 12–30 | 10 | 30–35 | [34,35,36,37] |
Scenedesmus species | 13–16 | 12–14 | 60–71 | [34,37,38] |
Dunaliella species | 3–17 | 14–21 | 48–57 | [27,34] |
Synechococcus species | 9–17 | 14–55 | 10–63 | [34,38] |
Euglena species | 14–18 | 14–20 | 39–61 | [34] |
Prymnesium species | 14–18 | 14–20 | 39–61 | [27,38] |
Anabaena species | 25–30 | 9–14 | 24–29 | [27,35,38] |
Chlamydomonas species | 2–17 | 9–21 | 28–56 | [27,34] |
Porphyridium species | 40–57 | 9–14 | 28–45 | [27,38] |
Arthrospira maxima | 13–13 | 6–7 | 60–71 | [27,34] |
Spirogyra porticalis | 33–64 | 11–21 | 6–20 | [38] |
Tetraselmis maculata | 15 | 3 | 52 | [27,38] |
Pavlovaceae | 6–9 | 9–14 | 24–29 | [34] |
Characteristics | Open System (Raceway) | Closed System (Photobioreactor) | References | ||
---|---|---|---|---|---|
Paddlewheel | Stirred Tank Reactor | Tubular Reactor | Column Reactor | ||
Light use efficiency | Good | Good | Best | Good | [55,61] |
Transfer of gas | Normal | Lower–higher | Lower–higher | Higher | [12,62] |
Mixing potential | Partial uniformity | Nearly uniformity | Perfect/absolute mixing | Partial mixing | [54,63] |
Control of species | Nil | Best | Good | Good | [55,64] |
Loss through evaporation | High | Moderate | Nil | Nil | [61,65] |
Quality of biomass | Variable | Reproducible | Reproducible | Reproducible | [54,57] |
Energy demand for mixing | Low | High | High | High | [64,66,67] |
Maintenance | Easy | Difficult | Difficult | Difficult | [62,64,67] |
Required space | Large area | Moderate | Moderate | Moderate | [54,57,63] |
Type of operation | Batch | Batch | Batch | Batch | [54,65,67] |
Setup capital | Low | High | High | High | [64,67] |
Limitations | Requires a huge area of land | Requires large setup capital | Possible formation of fouling/scale along the bend regions | High maintenance cost | [64,66,67] |
Production Technology (USD) | Capital Costs kg−1 (USD) | Labour kg−1 (USD) | Other Variable Costs (Utilities, Fertilizer) kg−1 (USD) | Total Costs/kg for a Large (100 ha–200 ha) Plant (USD) | Optimal Theoretical Total Costs kg−1 Dry Weight (USD) | References |
---|---|---|---|---|---|---|
Open ponds | 3.58 | 0.18 | 1.86 | 25 (2004) 7.07 | 0.81 | [43,68,69] |
5.87 | 0.25 | |||||
8–11 | ||||||
Horizontal tubular PBR | 3.25 | 1.04 | 1.09 | 4.92 | (NA) | [68,69] |
11.63 | 0.43 | 1.96 | 14.95 | |||
Flat panel PBR | 12.38 | 0.42 | 1.20 | 7.07 | 2.14 | [68,69,70] |
Crop | Greenhouse | M/Species | Extraction/Process Method | Conc. Of AE | Parameters | Reference |
---|---|---|---|---|---|---|
Lettuce | Soil | Chlorella vulgaris | Fresh and dried algal were applied in the field to vegetables | Biofertilizer—1/2, 1, 2, and 3 g of fresh algal and dry algal cells/1 kg soil Biomass | Chlorophyll a, b, and carotenoids. Plant growth (root dry wt. and length) | [138] |
Tomato | Petri plates | Acutodesmus dimorphus | 1 kg of biomass freeze dried submerged in distilled water, DW (Conc. 150 g L−1) = the suspension + micro fluidizer (M-110EH-30) = intracellular extract. Intracellular extract + centrifugation (8989× g/10 min/22 °C). The collected supernatant in a flask covered with foil paper to reduce potential degradation was stored at 4 °C | Seed primers—different concentrations (0, 1, 5, 10, 25, 50, 75, and 100%) of aqueous cell extracts from DW OR 10 mL, 0.1/9.9 mL, 0.5/9.5 mL, 1/9 mL, 2.5/7.5 mL, 5/7.5 mL, 7.5/2.5 mL, 10 mL | Seed germination, germination energy, lateral root development, flower development | [125] |
3 types of vegetable—Chinese Cabbage, Chinese broccoli, and Protea White Crown. | Tissue towel | Arthrospira platensis | A desirable quantity of microalgae suspension (50 mL) was removed from growing flasks and then allowed to pass through centrifugation for a maximum of 10 min. The collected supernatants were examined to determine the level of ammonia, nitrate, and nitrite | Biofertilizer—seed germination study—Arthrospira biomass. T1 to T5, T0 (tap water only). (2, 4, 6, 8, and 10 g L−1, respectively) biomass | Rate of germination, root and shoot length, vigor index as well as dry weight of 100 seedlings | [144] |
Arugula, Bayam Red, and Pak Choy plants | Potted plants experiment | Arthrospira platensis | A desirable quantity of microalgae suspension (50 mL) was removed from growing flasks. Then, it was allowed to pass through centrifugation for a maximum of 10 min. The collected supernatants were examined to determine the level of ammonia, nitrate, and nitrite | Biofertilizer—potted plants and control—Arthrospira platensis (5 g/500 g soil), inorganic fertilizer—Triple Pro 15/15/15 (3 × 10−1 g/500 g soil/week). Additionally, Arthrospira platensis + inorganic fertilizer (3 × 10−1 g/pot/week) biomass | Weekly measurement of plant growth (plant height and number of leaves per plant). After the completion of the experiment, parameters such as the number of leaves, the height of the plant, chlorophyll content, length of root, fresh, as well dry weights were determined. | [144] |
Tomato | Potted plants experiment | Anabaena vaginicola ISC90 and Nostoc calcicola ISC89 | Harvested biomass—DW was used to wash the cells. The cell extraction was carried out by grinding algae with a pestle and blender in DW. The final extract made up of 5.0 g fresh algae as the raw material submerged in 500 mL of DW is assumed to be a 1% extract | The final extract application was conducted by spraying the potted treated soil while the control was irrigated with water every 7 days. The arrangement of pots was a complete randomized design in a fully controlled experimental greenhouse. 1% extract/spray | The morphological parameters measured after 40 days of the experiment include plant height, root length, dry and fresh weight of plant, as well as the number of leaves | [140] |
Radish | Petri plates | BGA—Arthrospira platensis extract | Commercial dried biomass of SP used. Homogenate + centrifugation = supernatant considered to be 100% algal filtrate (1:10) | Foliar spray (5%, 7%, 10%, 15%, 20%, and 25%, v/v). Seed soaking—dose of 100, 300, 500, 700 μL per 1.5 g of seed | The longest and heaviest plant was observed at a dose of 300 μL/1.5 g seeds and 15% of filtrate as a foliar application. The chlorophyll content was higher at 100 μL/1.5 g seeds as well as 5% of filtrate as a foliar application. | [122] |
Rice | Potted plants experiment | BGA—Arthrospira maxima extract | Extracts obtained from three types of solvent viz. DW, methanol, and hexane at 0, 2.5, 3.5, 4.5, and 5 g L−1 of biomass/solvent | The potted plants were treated with extracts at three different stages of seed development, the dry stage, the radicle emergence stage, and the vegetative growth stage | DW, methanol, and extracts affect the germination of seed while hexane reveals no impact on seed germination. | [145] |
Wheat seeds | Petri plates | BGA—Arthrospira platensis extract | The seeds treated with extract were sown in a cotton base for the next 11 days, with nine replicates of each sample. | The coated seeds in three different doses (8, 14, and 20 μL g−1 of seeds) of formulation were used. Seed coated with 8 μL gave the best result | Seeds coated with the extract resulted in the increase in biomass yield by approx. 13% | [141] |
Tomato | Soil | 18 Microalgae and Cyanobacteria species from the AlgoBioTech collection | Screening of microalgae liquid extracts | Application doses of 0.1, 0.5, and 1 g L−1 were tested | The effects on plant growth, chlorophyll content, and nutrient uptake were significant | [146] |
Sugar beet | Hydroponic Hoagland solution | 1. Chlorella vulgaris 2. Scenedesmus quadricauda | Biomass of each species + was harvested by centrifugation + freeze-drying. The biomass + washed (distilled water)—final pellets + methanol (to lyse the cell wall) = intracellular extracts. Intracellular extracts + centrifugation + evaporation (organic solvent), the extract was collected with distilled water. | Growth promoter—2 mL L−1, 4 mL L−1 Extract/Hoagland | Root morphological analysis (total root length, root surface area, and the total number of root tips). Molecular analysis of root tissues | [139] |
Wheat | Soil Field trial | Arthrospira plantensis biomass and extract | As described in the work of Chojnacka et al. (2014) | Application doses of 1.0, 1.5, and 1.8 L ha−1 were tested | Quantity of grains per ear, the quantity of grain, and shank length | [72] |
Maize | Soil Field trial | Laurencia obtuse, Corallina elongate powder (biomass) | After collection, microalgae were washed, dried in shadow in the open air, and the drying process was completed in the oven at 60 °C for 5 h. The dried biomass was mechanically ground to the powdery form. | 3 g of powdered biomass of microalgae per kg soil. | Root improvement, Polyphenolic, and antioxidant contents | [142] |
Cucumber | Soil | Arthrospira platensis, Amphora cofeaeformis | Microalgae extracts were prepared as previously reported by Enan et al. (2016) [147] | Soil application—5 g m−2 Foliar application—2 g L−1 | Vegetative growth, yield, fruit quality, and nematode control | [143] |
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Bello, A.S.; Saadaoui, I.; Ben-Hamadou, R. “Beyond the Source of Bioenergy”: Microalgae in Modern Agriculture as a Biostimulant, Biofertilizer, and Anti-Abiotic Stress. Agronomy 2021, 11, 1610. https://doi.org/10.3390/agronomy11081610
Bello AS, Saadaoui I, Ben-Hamadou R. “Beyond the Source of Bioenergy”: Microalgae in Modern Agriculture as a Biostimulant, Biofertilizer, and Anti-Abiotic Stress. Agronomy. 2021; 11(8):1610. https://doi.org/10.3390/agronomy11081610
Chicago/Turabian StyleBello, Adewale Suraj, Imen Saadaoui, and Radhouane Ben-Hamadou. 2021. "“Beyond the Source of Bioenergy”: Microalgae in Modern Agriculture as a Biostimulant, Biofertilizer, and Anti-Abiotic Stress" Agronomy 11, no. 8: 1610. https://doi.org/10.3390/agronomy11081610
APA StyleBello, A. S., Saadaoui, I., & Ben-Hamadou, R. (2021). “Beyond the Source of Bioenergy”: Microalgae in Modern Agriculture as a Biostimulant, Biofertilizer, and Anti-Abiotic Stress. Agronomy, 11(8), 1610. https://doi.org/10.3390/agronomy11081610