Microalgae as Biofertilizers in Modern Agriculture: Comparison
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Due to the constant growth of the human population and anthropological activity, it has become necessary to use sustainable and affordable technologies that satisfy the demand for agricultural products. Since the nutrients available to plants in the soil are limited and the need to increase the yields of the crops is desirable, the use of chemical (inorganic or NPK) fertilizers has been widespread, causing a nutrient shortage due to their misuse and exploitation, and because of the uncontrolled use of these products, there has been a latent environmental and health problem globally. For this reason, green biotechnology based on the use of microalgae biomass is proposed as a sustainable alternative for development and use as soil improvers for crop cultivation and phytoremediation. 

  • biofertilizer
  • biorefinery
  • microalgae
  • modern agriculture
  • agriculture

1. Introduction

Because of the continued population growth, the food demand has increased, and the agricultural industry has changed, increasing the use of fertilizers to raise crop yields. In recent years, this sector has been forced to adopt an eco-friendlier approach [69][1]. According to Mitter et al. [70][2], biofertilizers are a sustainable approach to soil improvement for agriculture, and the term includes the use of single strains or a consortium of bacteria in formulations that when applied to soil they can improve its characteristics and plant growth. The viability of biofertilizers and their efficiency not only depend on the increase in crop yield, but also on the impact they can have on the soil—more specifically, the impact on the microbiological activity of the soil.
The most important element for the development of a plant is nitrogen. The content of N in the plant, alongside carbon, hydrogen, and oxygen, is the highest, and it plays an important role in the constitution of the plant structure, and it is present in chlorophyll, a pigment that has a direct impact on the photosynthesis processes, making it an essential element for the growth of the plants. The process of making this element bioavailable in the soil for plant usage is one of the main roles played by the soil microbiome: performing the fixation of atmospheric nitrogen. If the microbiome increases the content of nitrogen in the soil, the growth of the plants is maximized. Although it is considered that N2-fixation is only carried out by prokaryotic organisms like cyanobacteria, Clostridium, and Bacillus among others, this process can also be promoted by the addition of eukaryotic microalgae. It was shown that the application of the biomass of Chlorella vulgaris IPPAS C-1 with a sprinkler into bean crops showed an increased in the fixation of bioavailable nitrogen in the soil below the plant [7[3][4],71], making the use of microalgae as a natural source of N for the plants appealing.
Another chemical element important in the development of the plant is phosphorus. The P is present in the DNA and ARN bonds, and it even constitutes the molecule ATP fundamental for all the vital processes of the plant. The P that the plants require to function is normally obtained from the soil, and enriching it is one of the main goals for traditional fertilizers, but as mentioned in the last section, thihis can have detrimental effects on the soil and bodies of water, making it important to switch the P source for a less harmful one like the usage of microalgae. One way to solve the problem of P contamination in bodies of water and redirect this element to the soil is using microalgae to grow in said contaminated waters and applying the obtained biomass to the soil; this was carried out by Schreiber et al. [72][5], where he compared the effect of chemical fertilizers vs live and dry microalgae biomass on P bioavailability and the effect it can have on the growth of wheat plants. The results showed very similar plant growth between both types of fertilization with mineral fertilizer and microalgae. Although the concentration of P was lower in the plants fertilized with microalgae (both wet and dry), the similarities in root growth showed no difference between the treatments or even the positive control, demonstrating that the microalgae released N and P at a comparable rate as a traditional fertilizer.
Although biofertilizers using bacteria as the main component have been studied extensively, showing great results for a wide variety of crops [73,74][6][7], and the use of fungi-based biofertilizers is widespread too, the use of microalgae has gained strength as a versatile organism that can be used in a model of circular bio-economy in a wide range of industries from their employment for the biocapture of CO2 to their wastewater treatment to the production of food, energy, secondary metabolites, cosmetics, medicine, and even in the manufacturing of biofertilizers [75][8].
One of the benefits of using the three types of biofertilizers, apart from the plant growth promotion, is the endosymbiotic bond that the microorganisms create with the roots of the plants and the microbiome of the soil, improving the fertility by enhancing the water retention, soil structure, and the protection of the crops from pathogens and other pests, among other advantages [7][3]. The endosymbiotic bond is constructed by the ability of the bacteria, fungi, and microalgae-based biofertilizers to perform a variety of functions like the fixation of atmospheric nitrogen by bacteria and microalgae, the solubilization of phosphorus from these three types of microorganisms, and the release of nutrients that have shown a comparable result to the usage of traditional fertilizers, confirming the success of biofertilizers in agriculture [7,25][3][9]. Studies have shown that all the desired characteristics can be achieved with one strain of microalgae or cyanobacteria instead of using a consortium of bacteria or fungi to obtain the same results. One advantage of using microalgae-based fertilizers is decreasing greenhouse emissions by the sequestration of methane and CO2 while adding more organic carbon to the soil. All these benefits plus others can be achieved using microalgae as biofertilizers. However, one of the main drawbacks to their implementation on a larger scale is the lack of production on an industrial level and their commercialization, a problem that the traditional fertilizers and the biofertilizers based on bacteria or fungi do not have [25,76,77,78][9][10][11][12].
In Table 1, we present the comparison of the different types of biofertilizers commonly used against traditional fertilizers and microalgae-based biofertilizers, highlighting is presented, and the advantages/disadvantages, uses, and benefits in plant growth and the environment is highlighted.
Table 1.
Comparison of some characteristics of the traditional fertilizers against the three types of biofertilizers.
Characteristics Traditional Fertilizers Biofertilizers
Bacteria Fungi Microalgae/Cyanobacteria
Environmental damage by degrading the soil, water contamination, and eutrophication induction. ✔ x x x
Creation of symbiotic bonds with the plant roots and microorganisms within the soil. x ✔ ✔ ✔
Role in the nitrogen cycle making it available to the plant. x ✔ ✔ ✔
Promotion of the solubilization of phosphorus. x ✔ ✔ ✔
Soil fertility improvement. x ✔ ✔ ✔
The slow rate of nutrient release for the consumption of the plant x ✔ ✔ ✔
N fixation by individual strains, P solubilization, and hormone production for promoting the growth of the plant. x x x ✔
CO2 capture and greenhouse emissions reduction capability during the addition of organic carbon to the soil. x x x ✔
Industrial production and widespread used in the agriculture field. ✔ ✔ ✔ x
Table generated from the compilation of information from a variety of sources [7,25,76,77,78][3][9][10][11][12].

2. Microalgae-Based Bofertilizer

The use of microalgae as a soil enhancer/biofertilizer has a variety of benefits, not only for the environment but for the health of the soil and, consequently, for the crops. The percentages of moisture, pH, and light that are present when microalgae biomass is in direct contact with the soil cause the viable microalgae cells to become active and maintain their metabolic activity, aiding in the fixation of atmospheric nitrogen. This can also dose other macro and micronutrients important for the growth of the plants and can even create an endosymbiotic bond with the roots of the crops and other microorganisms present in the soil [62][13]. The symbiotic relationship between microalgae and plants has been studied, and Özer Uyar & Mısmıl [79][14] demonstrated the positive effects of growing a culture of Chlorella vulgaris and the mint plant Mentha spicata on a hydroponic system. They concluded that, among the different treatments, the co-cultivation of microalgae and plant, combined with aeration, had the greatest impact on the increase in plant weight because of the development of new shoots and leaves, and the measurement of the photosynthetic pigments on the plant revealed no stress on its growth. Another endosymbiotic bond of microalgae is with bacteria, making them thrive on different ecosystems taking advantage of one another to survive, making it a niche opportunity for the usage of this consortium in wastewater treatment, nutrient recovery, production of feedstock, biofuel, and biofertilizers [80][15]. It has been confirmed that the usage of microalgae and other microorganisms, even in harsh conditions like the desert, improves the fertility of the soil by enhancing its properties like water retention, maintaining its overall stability, and removing pollutants, and offering the plants a better substrate [81][16].
Among the benefits previously discussed, it is worth noting the important biomolecules for agriculture that can be found in microalgae; these biomolecules can improve plant productivity (biostimulants), provide plant protection against stress factors (biopesticides), and can improve soil characteristics (biofertilizers) [82][17]. Microalgae’s main contributions as soil enhancers are the changes in soil physical characteristics, the input of biomolecules, and the improvement in microbiological activity [83][18].
Microalgae-based biofertilizer contribution and effect on soils are related to the way microalgae gets into the soil and if the biomass is active or not, for example, if you are using fresh, dry, or digested biomass [7][3]. Based on that, the production of biofertilizers with microalgae could be relatively simple; in all cases, the first step will be microalgae biomass growth and harvest, and the differentiation will be after the harvesting, where the cells will be treated correspondingly to the type of biofertilizer formulation that is intended to have [73][6]. When the formulation of the biofertilizer/soil enhancer is liquid, the procedure is simple; the microalgae are grown and scaled up to an industrial level, and the obtained culture is supplemented with additives that aid to maintain the viability of the cells for longer periods [84][19]. On the other hand, if the biofertilizer formulation is expected to be solid, the procedure for obtaining it will require extra steps after microalgae biomass growth and harvest. These extra steps will mainly consist of the removal of water from the biomass by different techniques such as (i) lyophilization [85][20], (ii) air/oven drying, or (iii) carbonization [86][21].

2.1. Wet Microalgae-Based Biofertilizers

The simplest and the most low-cost way of using microalgae as a biofertilizer is to use the cells in suspension or the extract of all the biomolecules contained in them; this is considered wet microalgae and can be applied from the germination state of the seeds and for the cultivation on the soil. The performance of these treatments with microalgae extracts or living cells is further explored below.
In a study, Habibi et al. [87][22] germinated and cultivated three varieties of rice using a suspension of cyanobacteria Anabaena sp., and the researchers compared the results obtained from the cultivation supplemented with the blue-green algae vs the normal treatment with water. The results showed an enhanced germination process by all three varieties of rice used, and the plant growth showed a better performance than the control, leading the researchers to recommend the use of this cyanobacteria as a viable biofertilizer.
For a more rounded approach, Mahmoud et al. [88][23] aimed to determine the influence of two different microalgae strains, Chlorella vulgaris (Chlorophyta) and Anabaena cylindrica (Cyanobacteria), in the growth of Spinacia oleracea and to test if the microalgae supplementation, either by foliar or soil application, can decrease the accumulation of heavy metals on the spinach plant. Suspensions from both microalgae at 1 and 2% of dry weight used in both soil and foliar application were tested against spinach seeds planted onto heavy metal contaminated soils. The results showed that the microalgae suspensions promoted the growth of the spinach plant between 21 to 29% compared to the control; the best suspension occurred with Chlorella vulgaris at 2% and with the soil application for the growth, and it increased the macronutrients intake of N, P, and K of the plant while the treatment with Anabaena cylindrica at 1% concentration and foliar application performed better for a fresh and dry matter of the spinach and showed the best macronutrients intake compared to Chlorella vulgaris. In both cases, the microalgae reduced the heavy metal content of cadmium, lead, and copper, showing the capability of these microorganisms to accumulate these contaminants from the soil and stop them from entering the plant.
To prove the effects of microalgae as biofertilizers on different solutions, Kholssi et al. [89][24] studied the effect of three different solutions containing Chlorella sorokiniana biomass or extract of this microalgae on the growth of wheat compared to the usage of BG-11 medium as control. The three different solutions containing the extract and resuspended biomass in microalgae medium showed an increase in the germination process with the total weight of the plant and the length using solution 2, the one with only the filtered extract from the biomass, the best results of the experiment demonstrating that the extracellular biomolecules of the Chlorella sorokiniana are playing an important role for the cultivation of Triticum aestivum.
The difference in performance by dry and wet biomass compared to the usage of mineral fertilizers was tested by Schreiber et al. [72][5] by comparing the growth of Triticum aestivum by adding biomass and fertilizer to deliver between 115 to 130 mg of P per pot of plant. This experiment showed that, compared to the positive control with all the required nutrients for the growth of the plant, when the mineral fertilizer and wet and dry algae were applied to a nutrient-deficient substrate (Null Erde), the plant presented virtually the same weight in dry root and the root diameter. In the sand substrate, the best performance was observed by the mineral fertilizer, followed by the wet algae and, lastly, the dry algae in those same parameters as the previous substrate. This demonstrates that microalgae can be used as a biofertilizer with practically the same results, wet or dry; the only disadvantage is the cost of production of this biomass.

2.2. Dry Microalgae-Based Biofertilizers

Drying microalgae biomass is the most reported method for the production and application of biofertilizers. Retrieving the biomass by letting it air-dry directly into sunlight makes it the simplest, most effective, and cheapest way of obtaining a solid biofertilizer. Other ways of drying the microalgae cells are with lyophilization; although it is an effective method, the application of this at an industrial level is highly unlikely given the elevated cost of processing per sample. Some examples of the use of dry microalgae biomass using these drying methods as a growth enhancer for a variety of crops are presented below.
An experiment using solar-dried biomass of microalgae as a fertilizer with lettuce plants was carried out [90][25]. It was observed that the growth rate of the lettuce showed a 121% increase compared to the control (commercial fertilizer); in addition, when the amount of ammoniacal nitrogen was similar in the commercial fertilizer and the dry biomass of microalgae, the total nitrogen was 3.5 times higher in the dry biomass of microalgae. Similarly, commercial fertilizer was also used as a control, and the biomass of the microalgae Tetraselmis sp. was used as a biofertilizer, applied every 2 weeks at a dose of 0.5 g. This gave the best results in the diameter of the stem, number of roots, and length of leaves in date palm plants (Phoenix dactylefera) compared to the control [91][26]. Another study was conducted comparing the growth of Uruchloa brizantha using a commercial chemical fertilizer and a biofertilizer made with lyophilized microalgae (mainly C. vulgaris) compared to a control. The results indicated that the microalgae biomass was a good option as a fertilizer, showing similar plant productivity as the one treated with the chemical fertilizer [85][20]. Likewise, an experiment was conducted aiming to prove the efficacy of biofertilizers in the growth of spinach and baby corn. Of the six treatments, the one using the recommended dose of NPK through 100% of biofertilizer made with microalgae Mychonastes homosphaera (formerly Chlorella minutissima) (Chlorophyta) showed the highest yield of leaf biomass compared to the control and the dose of mineral fertilizers for the spinach; for the baby corn, the yield with and without husk showed the best results with the biofertilizer; and for the cob length, it showed similar results to the chemical fertilizer [92][27].

2.3. Hydrocarbon Microalgae-Based Biofertilizer

Hydrothermal carbonization, which converts biomass into hydrocarbon, is carried out at high pressures (above the water vapor pressure) and high temperatures (180–220 °C) in a liquid medium, for the treatment of biomass of microalgae, and it promises to be a good technique that provides excellent results in obtaining nutrients that can be found suspended in the liquid medium after the process, for example, nitrogen that is found mainly in the form of organic nitrogen, nitrates, and ammonium, or the orthophosphate that is formed from some polyphosphates present in the lignocellulosic raw material after the hydrolysis process [93,94,95][28][29][30]. In addition, biochar has been used as a biofertilizer or support material for the release of other fertilizers due to a series of positive effects it has on the environment, for example, higher profitability in the agricultural sector, restoration of degraded areas, and lower risk of eutrophication for the environment [96][31].
An increase in rice grain yield has been reported when fertilized with hydrocarbon from hydrothermal carbonization of C. vulgaris biomass thanks to the increase in ammonium ion NH4+ concentration in the soil after fertilization [86][21].

2.4. Biofertilizer Enhanced with Microalgae

Animal waste from cattle, pigs, and poultry generally has high nutrient values that are important for their use as fertilizer. These wastes cannot be directly treated with microalgae due to the presence of suspended solids and a high concentration of ammonium. Therefore, anaerobic digestion is carried out initially [97][32].
The bioavailability of nutrients has been studied when some corn digestates ensiled with dairy manure enriched with biomass of Chlorella sp. (10% of the total dry weight of the biofertilizer) in the growth of corn plants, giving greater value in the dry weight of the plant compared to the use of another genus of microalgae [98][33]. Suchithra et al. [99][34] also used the dry and macerated biomass of Chlorella vulgaris with cattle manure in the growth of tomato plants, giving excellent results, both in the useful life of the tomato, the size and in the concentration of nutrients, compared to the control (where the soil was not fertilized) and when C. vulgaris and cattle manure were applied separately. Another study was carried out with onion plants where growth, yield, leaf area, pigment content, and biochemical composition among other growth parameters were monitored, and it was found that the plant fertilized with cattle manure supplemented with S. platensis presented the highest growth factors analyzed, followed by the cattle manure supplemented with C. vulgaris, compared to the control [100][35]. A favorable result was obtained when the soil was treated with cow manure and two microalgae to analyze the growth of maize plants (length of leaf, root, dry, and fresh weight of the plant) for 75 days, as well as the content of macro and micronutrients and the yield of the plants, concluding that the best results were obtained when cow manure supplemented with Arthrospira platensis (formerly Spirulina platensis; Cyanobacteria)was used followed by the results obtained with cow + C. vulgaris [101][36].

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