Abstract
Due to intensive agricultural practices, agricultural lands are subject to continuous degradation. Agricultural productivity depends to a great degree on soil characteristics — soil is the substrate which when managed properly can support plant growth, but when abused requires additional inputs. Research is increasingly focused on the development of new non-synthetic and non-fossil-based products having less impact on the environment and health. In this context, the use of algae biomass (macro and micro) has been widely researched as a fertilizer for agricultural production as a “green economy” alternative product. Currently, the production of marine algae far outstrips the production of microalgae and its main use is for food consumption and some industrial applications. The cost of production is also variable, as marine algae are usually cultivated in integrated multitrophic aquaculture systems. The production of microalgae involves many variables, among them the species, the culture medium, obtaining process, final application, etc. and, based on these, its production cost is estimated. Some researchers point out that the use of simplified technology and increased production capacity tend to reduce operating costs within the ideal photosynthetic yield. This review sought to highlight the importance of algae and their extracts as natural biofertilizers and biostimulants, as well as the mechanisms of action and the possible relationship of these organisms with cultivated plants.
Highlights
• Macroalgae are potentially highly advantageous for sustainable agriculture.
• Microalgae can serve as biofertilizers or biostimulants.
• Algal extracts promote plant growth and nutrients uptake.
• The economic viability of biofertilizer production must be addressed.
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1 Introduction
1.1 Traditional and Contemporary Uses of Macro- and Microalgae
Macroalgae or (seaweeds) and microalgae, covered under the blanket term of “algae,” are a large and diverse group of organisms found preferentially in aquatic environments. With more than 156,000 described species, eukaryotic algae (both macro- and microalgae) are a rich source of biological diversity (Hughes et al. 2021). The macroalgae (seaweed) are multicellular organisms, present in both fresh- and saltwater, classified as green (Chlorophyta), brown (Phaeophyta), and red algae (Rhodophyta) (Overland et al. 2018). They are ecologically important because they help to provide oxygen to the sea and act as one of the main primary producers in the marine food chain (Chan et al. 2006). In recent times, seaweeds are increasingly gaining attention because they are perceived as being an environmentally friendly food, rich in nutrients, due to their contents of micronutrient minerals and vitamins (e.g., calcium, boron, zinc, potassium, phosphorus, magnesium, and several other trace elements) and the only plant-based sources of natural omega-3 long-chain fatty acids (Patel et al. 2021). Also, seaweeds can be used for feed additives, cosmetics, and dietary substitutes and additives, and other species are industrially processed to extract thickening agents such as alginate and agar (Chandía et al. 2004) or bioactive compounds such as lipids, proteins, minerals, carbohydrates, amino acids, antimicrobial compounds, osmoprotectors, and phytohormones (Patel et al. 2021), the latter of which are increasingly used in agriculture. Macroalgae (seaweed) are wild-collected as well as cultivated, and are primarily used as human food, being a traditional product in Asian food. Also, in coastal areas of Europe and the Americas, whether present on beaches or cultivated, seaweed is traditionally consumed and introduced in simple dishes as well as in the modernist kitchen and molecular gastronomy (Mouritsen et al. 2021).
Microalgae are photoautotrophic microorganisms with fast growth and good ability to adapt to different environmental condition (Ortiz-moreno et al. 2019). Microalgae, which comprise eukaryotic organisms and prokaryotic cyanobacteria (blue-green algae), are attracting growing interest because of their simple unicellular structure, high photosynthetic efficiency, ability for heterotrophic growth, adaptability to domestic and industrial wastewater, amenability to metabolic engineering, and potential for yielding valuable co-products (Chiaiese et al. 2018). Microalgae contain many compounds which serve at the biomolecular level for protection and survival in a marine environment. However, only a few microalgal species have been reported to have commercial value. This gap in knowledge of the chemistry produced by microalgae has generated interest in the biotechnology sector since microalgae have been reported to have applications in biofuels, cosmetics, nutraceuticals, and pharmaceuticals (Fernández et al. 2021; Khan et al. 2018; Porcelli et al. 2020). In addition, they can be used in the bioremediation of pollutants by purifying water and, removing heavy metals (Chatzissavvidis and Therios 2014) under pure or mixed strains purification. Algae play an increasingly important role in agriculture where they are used as biofertilizers (Grzesik et al. 2017; Haroun and Hussein 2003). In the literature, Algae play an increasingly important role in agriculture where they are used as biofertilizers (Grzesik et al. 2017; Haroun and Hussein 2003). Specialized metabolites, with promising biological activities, have been widely reported for seaweeds, and more recently for extracts from microalgae, because they maintain or regenerate agricultural soil fertility and also improve high productivity in agricultural crops (Hughes et al. 2021). These compounds are very interesting because they maintain or regenerate agricultural soil fertility and also improve high productivity in agricultural crops.
There is a changing paradigm in agriculture, shifting from focusing solely on direct nutrition to other functions which support plant growth in indirect ways, as well as protecting soil quality. Algae have a special potential in this regard, and since this is a novel field, this review aims to highlight the current state of knowledge to guide research and development. Due to the increasing use of algae-based biostimulants and biofertilizers, this review also highlights the role that algae (macro and micro) may play in maintaining soil fertility and stability, as well as the mechanisms of action and the possible relationship between these organisms and cultivated plants. In addition, the review provides a comprehensive overview of the global production of algae and the estimated cost of transforming algae biomass into biofertilizers.
1.2 Modern Applications of Algae in Agriculture: Focus on Microalgae
Due to intensive agricultural practices, agricultural land is subject to continuous degradation. Agricultural productivity depends essentially on the soil, which represents a substrate for plants and a fundamental resource that requires nutrients to be replenished. However, research is gradually more focused on developing new natural products from aquatic environments with the same efficacy as some synthetic products, but with less impact on the environment and health (Dineshkumar et al. 2018). The use of algae or its extracts as fertilizer can then meet the global challenges of using non-toxic and biodegradable products (Dhargalkar and Pereira 2005; Prakash and Nikhil 2014).
Though an age-old practice, the available information in the literature refers to the application of fresh or dried and chopped seaweed as a soil amendment to enrich plants with nutrients, hormones, and metabolites resulting in increased growth (Prakash and Nikhil 2014; Uysal et al. 2015; Vasileva et al. 2016). Records show that brown algae are generally richer in potassium and the most widely used in agriculture such as, Turbinaria spp., Laminaria spp., Fucus spp., and Sargassum spp. (Hong et al. 2007; Ugarte et al. 2006). Microalgae (such as Scenedesmus, Chlamydomonas, and Chlorococcum) and cyanobacteria have a better capacity to perform a high number of N-transforming reactions compared to other soil microbes (Xiao and Zheng 2016). They allow nitrogen fixation and the accumulation of inorganic phosphate and the production of polyphosphates (Mukherjee et al. 2015; Whitton et al. 1991; Xiao and Zheng 2016). Consequently, the positive effects of algae and their derivatives in agriculture include the resistance of plants to pathogens, tolerance to various stresses, improved seed germination, growth of root systems, and increased plant yield (Chatzissavvidis and Therios 2014; Eyras et al. 1998; Kuwada et al. 2006). The production of microalgal/cyanobacterial biomass can be quite advantageous, when compared to the production of other biological resources. Production systems pose little competition with food production since microalgae can be cultured in non-arable areas and have low requirements for freshwater and nutrients since microalgae can grow in low-quality waters such as wastewaters. Additionally, many species of microalgae and cyanobacteria have the ability to uptake CO2 from the atmosphere, thus reducing the carbon footprint of agricultural practices (Gonçalves 2021).
Uysal et al. (2015) revealed that microbial fertilizers obtained from microalgae increased soil organic matter and water retention capacity. Recently, Abinandan (et al. 2019) investigated the ability of these beneficial microorganisms in maintaining soil fertility and health. Nevertheless, microalgae and cyanobacteria are associated with the development of the top layer of the soil, called “biological soil crusts” and the formation of soil biofilms, which can be triggered by inoculation of soils with one or more organisms (Manjunath et al. 2016; Marks et al. 2017; Rossi et al. 2017). The potential of cyanobacteria and microalgae for stabilization and recovery of degraded soils have been well documented in a number of reviews, as they have been shown to be effective in increasing fertility, stability, and recovery of natural soils, agricultural, burnt areas, and desert areas (Chamizo et al. 2018; Chen et al. 2013; Chock et al. 2019; Wang et al. 2009; Wu et al. 2013; Zaady et al. 2017).
2 Macro- and Microalgae Fertilizing Products on the World Market
In agriculture, soil fertility and health soil are key for productivity, which varies according to soil properties in addition to precipitation and temperature (Cong and Brady 2012). The use of commercial fertilizers has generated impacts on the environment that are increasingly visible and, taking these into consideration, new forms of fertilization are under evaluation in order to minimize negative impacts while maintaining productivity. Among them, the use of algal biomass in the soil stands out.
According to the most recent data provided by the Food and Agriculture Organization of the United Nations (FAO), algae world aquaculture production in wet weight reached 32.4 million tons, which is in monetary terms equivalent to USD 13.3 billion (FAO 2020). Global production of farmed aquatic algae is dominated by marine macroalgae, in contrast to microalgae production which comprises a low portion (FAO 2018a).
Farmed seaweeds corresponded to 97.1% of the total volume produced in 2018, and that year the production lightly fell by 0.7%. Nonetheless, farmed seaweeds have tripled up from 10.6 million tons in 2000 to more than 31 million tons in 2015; subsequent years recorded slower growth until 2018, about 31.6 to 32.4 million tons per year. East and Southeast Asian countries are the largest producers, with major producers being China and Indonesia with 57.1 and 28.8% of the market share, respectively, followed by Republic of Korea, Philippines, and another ten countries summing to just 14.1% of the remaining production (FAO 2020).
The most popular farmed seaweed specie is Japanese kelp (Laminaria japonica) with more than 11.4 million tons produced in 2018; this is consumed as food in dried or pickled form. The second most produced are the tropical seaweeds Eucheuma spp., with 9.2 million tons, used for food processing as well as an ingredient in cosmetics and as raw material for carrageenan extraction. Next are the Gracilaria seaweeds (Gracilaria spp.), Wakame (Undaria pinnatifida), Nori nei (Porphyra spp.), and Elkhorn sea moss (Kappaphycus alvarezii), used in traditional food and some of them in industrial applications, with an annual production between 4 and 1 million tons (FAO 2020).
Seaweed farming is gaining increasing attention to be promoted and monitored for climate and environmentally friendly bioeconomy development around the world (Duarte et al. 2017). However, in agriculture, the application of seaweeds as fertilizers has been very common since ancient times, especially in coastal areas (Mukherjee and Patel 2020). Their use involved the direct application of a liquid solution over the soil, then seaweeds were dried and powdered for easy application. Although the popularization of chemical fertilizer products in the middle of the last century stagnated their use, lately seaweed extracts have become an important alternative in sustainable agriculture (Shah et al. 2013). The fertilizers that are derived from seaweeds are known as new generation fertilizers, containing considerable amount of nutrients which are easily absorbed by plants, and the extracts are used in different ways like seed treatment, foliar spray, and soil application for plant protection and for plant growth promotion (Verma et al. 2020).
Some studies have estimated the cost of production of different seaweeds as part of an integrated multi-trophic aquaculture system, reporting a wide variety of results about its cost-effectiveness. In commercial terms, producers claim that production costs of Saccharina latissima are less than €10–38/kg N removed (Holdt and Edwards 2014). The global seaweed industry has produced more than US$ 6 billion per year and of this amount, 85% comes from its use for food production, and the rest proceed from other industrial applications such as cosmetics, animal feed additives, and fertilizers (FAO 2018b), whereas it is noted that the latter is a growing industry.
In 2018, the microalgae production recorded by FAO were about 87 thousand tons produced from some countries such as Australia, China, Czechia, France, Iceland, India, Israel, Italy, Japan, Malaysia, Myanmar, and the USA. Nonetheless, 86.6 thousand tons was reported from China alone; hence, the FAO data understate the real scale of world microalgae farming because of unavailable data from important producers (FAO 2020).
There are many variables involved in the production process to obtain microalgae biomass, among them is the algae species, wastewater or nutrient influent, culture medium, final application, obtaining process, current available technology, etc. (Acién Fernández et al. 2019). Thus, the production cost depends on all aspects of that process. Some studies carried out to find the most efficient process estimated that the production cost of high value microalgae biomass was 69 €/kg, from tubular photobioreactors operated in continuous mode, with an annual production capacity of 90 t/ha/year. Simplification of the technology and scale-up to a production capacity can allow to reduce the production cost up to 12.6 €/kg. Nonetheless, to achieve an economically feasible process requires a substantial reduction of the current costs and to operate them near the optimal photosynthetic yield (Acién et al. 2012).
Other authors affirm that the key is scaling up the microalgae production, which has a very large impact on the cost. Based on the state-of-the-art technologies to produce microalgae for aquaculture, a cost reduction of 92% could be achieved by changing the scale from 25 to 1500 m2, resulting in a cost of 43 €/kg, producing 3.9 t/year for tubular reactors in a greenhouse (Oostlander et al. 2020).
Regarding agriculture application, another study demonstrates that microalgae biomass production systems are viable technically and economically for the purification of wastewater effluents, producing fertilizer products and biomass for livestock feed. The analysis carried out shows that is more versatile and cost-friendly to reduce digestate turbidity through electro-flocculation method, which has a cost of 0.63 €L−1 (Miñón Martínez 2017).
One of the most expensive process steps is the biomass recovery from the culture medium — harvesting the microalgae may contribute to 20–30% of the total biomass production cost (Molina Grima et al. 2003). It is crucial to understand how to select the right algae species, create an optimal system, and build a cost-effective cultivation unit that can precisely deliver the formula to each individual algae cell, no matter the size of the facility, or its geographical location (Mata et al. 2010).
3 Role of Macroalgae (Seaweed) in Agriculture
Seaweeds are used since antiquity for agricultural applications and current demands of organic agriculture and organic food have considerably encouraged the use of organic treatments including seaweed extracts in agriculture (Nabti et al. 2016). Given its characteristics and the presence of several beneficial components in marine algae, research has been developed aiming at the potential contribution to crop growth and productivity through the modulation of metabolic pathways (Craigie 2011). Thus, increasing attention has been focused on marine-based sources.
The use of algae as a biofertilizers has many benefits, such as stimulating seed germination and enhancing plant health and growth, namely root and shoot elongation (González-Pérez et al. 2022). Moreover, other beneficial effects of seaweed extract applications on plants include better absorption of water and nutrients, resistance to frost and salt, enhancement of the growth of beneficial soil microbes, and enhancing abiotic stress tolerance and defense against pests, diseases, and microorganisms (Chai and Schachtman 2022).
Different fertilizers based on seaweeds are available on the market such as liquid fertilizers and a powder from seaweed manure (Patel et al. 2021). The use of liquid seaweed extracts as foliar applications has been shown to be potent in increasing the growth of many crops, including various herbs, grains, flowers, and vegetables (Kocira et al. 2018; Patel et al. 2021). The brown seaweed Ecklonia maxima collected from the Atlantic coast of South Africa is extensively used as a seaweed liquid additive (Stirk et al. 2014a). Currently, the fertilizers produced from seaweed extracts introduced in the 1950s have reached a wider use and market than seaweed and seaweed meal because of their easy utilization (Renaut et al. 2019), and is also likely related to ease of distribution, concentration of active substances, and factors such as shelf life.
Currently, the increasing number of studies evaluating the importance of seaweeds for their utilization in agriculture field confirms the potential of this organism in the preparation of the extracts used in plant health products and fertilizers.
4 Role of Microalgae in Agriculture
The importance of microalgae in soil formation, improvement of fertility, and increasing crop productivity cannot be underestimated in achieving world food security (Adesalu and Olugbemi 2015; Li et al. 2017; Liu et al. 2017). Microalgae act in the decomposition of organic matter, participating directly in the biogeochemical cycle of nutrients and, consequently, mediating their availability in the soil (Balota et al. 1998; Nayak et al. 2019), in addition to degrading toxic substances (Priya et al. 2014). The use of microalgae biomass can be advantageous because it is rich in nitrogen, as well as benefits of carbon sequestration, improved soil health, soil water retention, stability of soil aggregates, and prevention of nutrient losses (Solé-Bundó et al. 2017).
The application of microalgae biomass to the soil has been investigated and the results point to improvements in chemical characteristics, in the increase of the microbial community, respiration, and photosynthetic activity, in addition to the capacity for bioremediation of pollutants. Currently, research has focused on developing various techniques for introducing microalgae into agricultural production (Alvarez et al. 2021). As described above, microalgae have generated interest due to their great adaptability to various nutrient substrates and their ability to grow under different environmental conditions (Chiaiese et al. 2018; Safi et al. 2014). Due to their phototrophic nature, they contribute to carbon emissions reduction, and may even have a role in soil carbon sequestration since they increase soil organic matter (Jeong et al. 2003; Renuka et al. 2018; Sayre 2010). Microalgae, in addition to being found in aquatic environments, also occur in terrestrial environments and are encountered both on soil surface and within the soil profile (Mathushika and Gomes 2022). This interesting group of microorganisms has applications in modern agriculture since they maintain and release nutrients in plant-assimilable forms, increase soil organic matter levels, and indirectly enhance plant growth and crop yields through stimulation of soil microbial activity (Marks et al. 2019; Renuka et al. 2018).
4.1 Direct Fertilization vs. Indirect Effects
Microalgal biomass is effective for soil fertilization since it releases nutrients into the soil in a form that is adequate for roots and at an appropriate rate (Schreiber et al. 2018); in this sense, their potential nutrient use efficiency can be greater than many chemical fertilizers (Coppens et al. 2016; Mulbry et al. 2005; Renuka et al. 2016; Volf and Rosolem 2020), which can result in less environmental pollution and a higher rate of nutrient utilization. Research has shown that microalgae may be employed as an organic slow-release fertilizer (Coppens et al. 2016; Mulbry et al. 2005, 2007) through a gradual release of N and inorganic P from organic P-compounds in soil to meet plant demands (Mulbry et al. 2007; Ortiz-moreno et al. 2019). Many detailed studies examining the effects of eukaryotic microalgae on soil in terms of impact on some hydrolytic enzymes show that inorganic P concentrations are increased due to increased phytase activity (Zhu and Wakisaka 2020). Microalgae have the ability to fertilize soil through polysaccharides and mucilage’s secretions, which serve as C source (Karthikeyan et al. 2007; Kholssi et al. 2018; Ortiz-moreno et al. 2019). The application of microalgae leads to increased plant growth, reduces effects of saline stress on plants, and increases crop production (Chanda et al. 2019; Elarroussi et al. 2016).
Indirect effects and special applications are also of note: organic fertilization, with the application of microalgae biomass, can affect the biomass, activity, and structure of soil microbial communities through the modification of physical and chemical characteristics (Alvarez et al. 2021; Renuka et al. 2018; Shi et al. 2018). In addition to these characteristics (Ahmad et al. 2017; Cooke and Mouradov 2015; Priya et al. 2014), with microalgae comes the capacity for bioremediation of metallic and organic pollutants. Microalgae contain bioactive compounds and are capable of improving growth (Chanda et al. 2019; Chiaiese et al. 2018; Renuka et al. 2018) and increase the activity of enzymes that participate in the release of nutrients required by plants (De Caire et al. 2000; Rai et al. 2019).
4.2 Microalgae Applications Involving Whole or Viable Cells
Soil health is crucial for sustainable agriculture, and applications of biofertilizers increasing biomass and activities of the microbiota have indirect effects on the availability of soil nutrients and biological processes (Marks et al. 2019). Microalgae applications involving whole or viable cells are differentiated from extracts of algae (biostimulants, next section) since the methods of application may differ and can be used to promote certain outcomes. For horticultural and agronomic crops, their targeted applications have been adopted, depending greatly on the microalgal product and formulation. The application of microalgae as fertilizers includes (i) soil amendment with algal formulations using ideal carriers, (ii) soil amendment with algal dry biomass or suspended liquid culture, and (iii) foliar spray or substrate/soil drench with algal culture (Chiaiese et al. 2018; Coppens et al. 2016; Renuka et al. 2018). Chlorella vulgaris, Chlorella fusca, and Spirulina platensis have been used for various plants such as tomato, cucumber, onion, lettuce, and pepper cultivation with a view to promote their production with marketable quality (Elarroussi et al. 2016; Kim et al. 2018; Rachidi et al. 2020; Zhang et al. 2017).
Al-Maliki and Breesam (2020), assessing, in corn cultivation, the interactions between arbuscular mycorrhizal fungi (Glomus mosseae), algae biomass (Chlamydomonas sp.), and subsequent effects on carbon mineralization, bacterial biomass carbon, soil pH, root density, among others, detected that combination of AM fungi with algae caused carbon decomposition and formation of soil aggregates, reducing pH and increasing bacterial biomass C (carbon), as well as root density. Liu et al. (2019) evaluated in rice fields whether it influences the composition of the biofilm community and whether it drives phosphorus immobilization at the soil–water interface and found, among other conclusions, that the increase in soil organic carbon (SOC) and total nitrogen (STN) is responsible for the great diversity of algae, with dominance of the production of chlorophytes and exopolysaccharides (EPS), and that this scenario allows the increase of phosphorus assimilation and adsorption by phototrophic biofilms in rice fields. Using microalgae in microcosms, Marks et al. (2017) found that in treatments with algae application, soil respiration was increased, and the development of a stable community of eukaryotic and prokaryotic microorganisms on the soil surface was accelerated. Moreover, studies have shown that the growth of several plants was enhanced where microalgae are used (Grzesik and Romanowska-Duda 2014; Kholssi et al. 2018; Mukherjee et al. 2015, 2016; Mulbry et al. 2005; Schreiber et al. 2018). Whether applied fresh as live cell suspensions (Alvarez et al. 2021) or even dried, studies have cited increases in root hair length when compared to the mineral fertilizer (Schreiber et al. 2018). Grzesik et al. (2017) indicated that foliar application with freshwater microalgae such Chlorella sp. produced an increase in growth and physiological activity of willow plants (Ortiz-moreno et al. 2019). Table 1 is an overview of studies carried out in the most important algal strains at laboratory or greenhouse scales, showing the effects of application of cell suspensions (fresh biomass) or dried algal biomass on plant growth.
Besides their effect of enriching soils with essential nutrients and improving plant growth, recent studies have shown that application of photosynthetic algal suspensions not only enhances plant growth but also helps in improving soil biological quality through increasing eukaryotic and prokaryotic biomass and the activities of heterotrophic microorganisms in the soil (Marks et al. 2017). Many other authors have already demonstrated modification of soil microbiota by some cyanobacteria, whose prolific production of extracellular polymeric substances serves as a carbon source for bacteria in the rhizosphere (Manjunath et al. 2016; Priya et al. 2014; Xiao and Zheng 2016). An improvement in the soil structure may be due to the number of polysaccharides such as alginates and fucoidan present in the algal extracts. These can join to metallic ions in soil and help in gel formation, which leads to a better water retention and aggregate structure (Khan et al. 2009). This also facilitates the development of a strong root system that is responsible for nutrient uptake. Increases in the soil indigenous microbial population using N2-fixing cyanophyte Nostoc muscorum were confirmed as well by Rogers (1994), with numbers of bacteria 500, fungi 16, and actinomycetes 48 times compared to non-inoculated soil on day 300. Renuka et al. (2017) evaluated the potential of wastewater-grown microalgal consortia in enhancing the soil micronutrient availability and uptake in wheat crop detected a strong positive correlation and was recorded between the availability of micronutrients in soil at mid-crop and grain yield.
5 Algae-Based Biostimulants
The European Biostimulant Industry Council (EBIC) defines a biostimulant as a material whose content function when applied to plant or soil is to stimulate natural processes to improve nutrient uptake or efficiency and improve abiotic stress tolerance and crop quality, regardless of its nutrient content (Ricci et al. 2019). Use of seaweeds as a fertilizer has been common historically (Mukherjee and Patel 2020), but their recently discovered role as a biostimulant is a new way to understand agricultural applications of these organisms. The growing environmental concern in agriculture, which entails that high production has to be sustainable and minimize its environmental impact, is the reason why the study of algal extracts as biostimulants products is one of the main directions of algae biotechnology (Shekhar et al. 2012). Macroalgae (seaweed) and microalgae have been considered a rich source of plant biostimulants, with macroalgae being more exploited, because for microalgae, although known to have positive effects on crop development, growth, and yield, their commercial implementation is limited due to lack of research and production cost (Kapoore et al. 2021). Even though algal extracts have lately been gained interest in crop production because of their stimulatory effects, the mechanisms underlying these benefits are still unclear (Tan et al. 2021). Seaweed concentrates are typically applied in low doses and show a growth-promoting effect due to their content in plant growth regulators, mainly auxins, brassinosteroids, cytokinins, gibberellins, and abscisic acid (Reed et al. 1998; Nguyen et al. 2020), but also some other purified compounds present in the commercial algae products are laminarin, alginates, carrageenan, polyanionic substances (Du Jardin 2015), abscisic acid, gibberellins, amino acids, betaines (Michalak and Chojnacka 2015), and brassinosteroids (Stirk et al. 2014b). They can be applied directly to plants as a foliar treatment or as a solution to soil. The resulting plant growth promotion could be the result of its synergistic effect (Santner et al. 2009). Table 2 details these main compounds and its application effect.
Several mechanisms have been proposed to explain the improvement shown in terms of nutrient content, plant growth, and higher yield by the application of algal extracts. These can be divided between mechanisms affecting the soil or the plant physiology. Applications targeting plant physiology and biochemistry will usually be applied as a foliar spray, but may also include inoculation of roots or seeds or soil, while applications for improving soil properties are applied as soil drenching.
5.1 Biostimulant Applications Targeting Plant Physiology
There are several studies carried out both in the field and in the greenhouse that show the plant biostimulant properties of algal extracts. Du Jardin (2015) reported that seaweed extract is considered as a natural and organic plant growth stimulant due to its effects on enhancing nutrition efficiency, abiotic stress tolerance (more in following section), and/or crop quality traits. In relation to the literature focused on studying nutrient uptake and plant growth, Almaroai and Eissa (2020) conducted a 2-year field experiment to study the effect of different doses of foliar application of marine algae (Amphora ovalis) extracts on onion. The results showed that the highest dose of the algal extract increased N (nitrogen), P (phosphorus), and K (potassium) uptake by the onions compared to the unsprayed plants. In relation to the literature focused on studying nutrient uptake and plant growth, Turan and Köse (2004) tested the foliar application effect of three algal extracts’ commercial products on grape nutrient uptake. These products showed a significant increase in the Cu uptake when the nutrient availability was low. When in optimal conditions, uptake of the following improved: N, P, K, Ca (calcium), Cu (copper), Fe (iron), Mg (magnesium), Mn (manganese), and Zn (zinc). Rathore et al. (2009) observed an increment of N, P, K, and S (sulfur) concentration in soybean when Kappaphycus alvarezii extracts were foliar applied. This improvement was positively correlated with the dose, with the largest nutrient concentration in the treatment that received the highest dose. Merwad (2020) applied an Ascophyllum extract on wheat under salinity stress and observed a higher straw and grain yield, plant height, and protein content compared to control. Crouch et al. (1990) measured the effect of a commercial algal extract on lettuce growth and Ca, Mg, and K uptake. They reported an enhanced plant growth and nutrient uptake when the plants were also receiving an optimal nutrient solution. Nelson and Van Staden (1984), using the same commercial product, showed a significant increase in root growth and higher N and P content compared to the control treatment. Several studies have reported that plants treated with seaweed extracts had higher mineral contents compared with non-treated plants (Di Filippo-Herrera et al. 2019; Mahmoud et al. 2019; Mikhailyuk et al. 2014).
El-Aziz Kasim et al. (2016) reported that priming of seeds with seaweed extracts enhanced the photosynthetic pigment content in leaves of radish plant. On the other hand, Mahmoud et al. (2019) demonstrated that the application of seaweed extracts led to an enhancement in leaf pigment contents of chlorophyll a, chlorophyll b, chlorophyll a + b, and carotenoids. Similarly, in other studies, the author observed that the application of seaweed Pterocladia capillacea liquid extract improved the concentrations of chlorophyll a, chlorophyll b, and carotene in Jew’s mallow during two successive seasons (Ashour et al. 2020).
Mahmoud et al. (2019) showed that the content of total flavonoids, total phenolics, and anthocyanins in leaves and roots of red radish plants was higher with brown seaweed extract-soaked seeds than water-soaked seeds during the two successive seasons. In previous studies, the authors found that the accumulations of bioactive compounds and antioxidant activity were improved when the brown seaweed was utilized of as biofertilizer, thus increasing the nutritional value of treated plants (El-Aziz Kasim et al. 2016; Uma Maheshwari 2017).
Rayirath et al. (2009) have tested the applicability of using Arabidopsis thaliana as a model to study the activity of two different extracts of algae from A. nodosum and the results of this study suggest that extracts of A. nodosum affect the root growth of Arabidopsis at very low concentrations (0.1 gL−1), whereas plant height and number of leaves were affected at concentrations of 1 gL−1over control plants. Mahmoud et al. (2019) observed the effect of brown seaweed extract of Sargassum vulgare as a natural plant growth stimulant used as a pre-sowing seed soaking. The results indicated that the application of Sargassum vulgare led to greater plant height, number of leaves or plantlets, root diameter, and fresh and dry weights of leaves and roots. In addition, authors reported a direct correlation between foliar spraying of seaweed extract and the enhancement of plant vegetative growth plants (Garai et al. 2021).
González-González et al. (2020) also found out an increased root length and weight along with higher protein concentration in tomato when a seaweed extract was applied. They also reported a synergistic positive effect in the plant when an arbuscular mycorrhizal fungus and the seaweed extract were applied together. Supraja et al. (2020) tested different doses of a mixed consortium of microalgae consisting mainly of Chlorella sp., Scenedesmus sp., Spirulina sp., and Synechocystis sp. This mix was characterized in terms of carbohydrates, proteins, and lipids and was applied as a foliar spray to tomato plants and as a seed primer to tomato seeds. Treated seeds showed a faster germination rate and a faster plant growth. Both applications resulted in a higher total plant height, root length, and biomass content compared to control. Kumar and Sahoo (2011) tested a seaweed liquid extract of Sargassum wightii on the germination rate, growth, and yield of Triticum aestivum. They observed an enhanced growth, yield, and seed germination when a low concentration of the extract was applied. Michalak et al. (2015) used microwave-assisted extraction to acquire liquid extracts from Baltic seaweeds. Results showed higher height, weight, chlorophyll, and micro- and microelement content in treated plants in comparison to the control group. Yao et al. (2020) showed the ability of seaweed extracts to improve yields, leaf photosynthesis, ripening time, and net returns of tomato (Solanum lycopersicum Mill). Spinelli et al. (2010) noted that a commercial extract from Ascophyllum nodosum could be used to replace sequestrene, a standard iron chelate.
An increase in the root shoot ratio has been observed in several crops, regardless of a foliar or a soil application of the extracts. This effect has been reported in cucumber, tomato, barley, raspberry, and bean (Nelson and van Staden 1984; Spinelli et al. 2010; Steveni et al. 1992; Stirk and Van Staden, 1997). Lastly, also reported is promotion of the symbiotic relationships between mycorrhizal fungi and plant roots. This type of fungi plays a very important role in nutrient uptake. The application of algal extracts has shown an increased growth and infection rates of these fungi (Khan et al. 2009). Kuwada et al. (2006) reported that extracts from Gracilaria verrucosa, Gelidium amansii, Eucheuma cottonii, and Chlorella pyrenoidosa successfully stimulated Gigaspora margarita and Glomus caledonium growth in papaya and passion fruit. Other proposed mechanisms regarding the plant physiology include the modulation of root exudates to benefit plant growth–promoting rhizobacteria (PGPR) and growth of other friendly microbes (Chatzissavvidis and Therios 2014).
5.2 Biostimulant Applications to Soil
Application of seaweeds and seaweed extracts improves soil moisture-holding capacity by promoting the growth of beneficial soil microbes which triggers the secretion of soil-conditioning substances by these microbes (Khan et al. 2009). In addition, it may be possible that the algal extract application increases micronutrient availability due to chelation phenomena by the largest organic molecules (Halpern et al. 2015). Research by Ashour et al. (2020) with the brown seaweed M. pyrifera and E. arborea has shown that liquid seaweed extracts can increase soil nutrient content and crop yields for some cultivated plants as they contain micro- and macro-elements which are beneficial for growing plants. Barone et al. (2019) evaluated the effect of Chlorella vulgaris, Scenedesmus quadricauda, or their extracts applied directly into the soil, by monitoring the complex soil-microorganism-plant system showed that both positively affected soil biological activity by increasing values of the biochemical index of potential soil fertility both in cultivated and uncultivated soils.
5.3 Biostimulants and Stress Tolerance
In relation to the role of algal extracts in the enhancement of stress tolerance, several studies have been carried out aiming to observe the effect of its application to different crops (Van Oosten et al. 2017), since algal extracts are known to protect the plant against a biotic/abiotic stress (Michalak et al. 2017). Mansori et al. (2015) attribute this protection against stress to a higher phenolic content, while Shukla et al. (2018) attribute it to an increase in antioxidant activity or even a regulatory role in responsive gene expression. Most of the literature has focused on the study of these products against drought, salinity, or high temperature conditions, but little is known about these effects facing nutrient unbalance and the mechanisms underlying (Carrasco-Gil et al. 2018).
Rayirath et al. (2009) tested the ability of different organic sub-fractions from an A. nodosum extract to promote freezing tolerance of Arabidopsis thaliana, reporting that the lipophilic sub-fractions were the ones increasing this tolerance. Mansori et al. (2015) studied the effect of the red algae Ulva rigida and brown algae Fucus spiralis on drought stress tolerance in green bean plants (Phaseolus vulgaris L.). The results revealed that treatment with seaweed extract improved plant growth with and without drought stress conditions in bean plants. Bradáčová et al. (2016) used extracts containing Zn and Mn which were shown to enhance cold stress tolerance, and the authors concluded that their seaweed extract was effective thanks to the increase in those microelements. Carrasco-Gil et al. (2021) investigated tolerance to an Fe deficiency stress in tomato when different compounds from algal extracts were applied in different doses. They reported that the lowest dosage of phenolics, laminarin, and fucose compounds helped to alleviate this stress. Regarding salinity stress, Bonomelli et al. (2018) found that the application of A. nodosum extracts could alleviate the plant growth suppression caused by saline stress in avocado plants, but only at an early stage. Hussein et al. (2021) tested the impact of seaweed liquid extracts on seed germination of Zea mays and Vigna sinensis, finding a positive correlation between the application of these extracts and higher germination indices, higher growth of seedlings, and reduce the effect of seawater supplementation.
Finally, a considerable number of recent studies have demonstrated that algal extracts can be used to lessen the effects of drought on crops. Martynenko et al. (2016) measured the survival of soybean during 5 days in a drought assay. Leaves from plants treated with a commercial seaweed extract did not wilt (as was the case in the control treatment) and had a better survival rate after rewatering on the fifth day. Santaniello et al. (2017) applied A. nodosum extracts as a pre-treatment to Arabidopsis plants, helping the plant to cope with the stress conditions and improve its water use efficiency.
5.4 Commercial Biostimulants
“Maxicrop” was the first liquid seaweed extract derived from fresh Norwegian kelp (Ascophyllum nodosum) for agricultural use. It was developed in the late 1940s and used for years by organic farmers for its many plant health benefits (Craigie 2011). Currently, there are many other liquid and powdered seaweed extracts based primarily from brown seaweed that are sold as plant biostimulants (Khan et al. 2009). In addition, another commercial biostimulant used in agriculture made from the kelp Ecklonia maxima was reported to promote different responses including greater resistance to abiotic and biotic stressors, enhanced root and shoot growth, and higher yields (Stirk et al. 2014a). The polyamines (putrescine and spermine) and ethylene precursor 1-aminocyclopropane-1-carboxylic acid have also been detected in Kelpak® (Nelson and van Staden 1984). Papenfus et al. (2013) demonstrated that Kelpak® improved root growth and thus the higher seedling vigor of nutrient-stressed okra seedlings. In another work, it was found that other groups of plant growth regulators like abscisic acid, gibberellins, and brassinosteroids were present in seaweed extract Kelpak® (Stirk et al. 2014b). Until now, many seaweed extracts are available on the market as commercial products for their utilization for plants: Ekologik R (Chile), Kelpak 66 (South Africa), Maxicrop (UK), Seasol (Australia), Goemill (France), Seamac Ultra Plus Liquid and Turfcomplex (UK), SeaCrop16 (USA), Algamino Plant (Poland), Actiwave R (Italy), and Acadian (Canada) (Khan et al. 2009).
6 Conclusions
Macro- and microalgae contain an incredible wealth of bioactive compounds, some of which are already available in commercial products, and are already playing a role as environmentally friendly bio-based fertilizers. There are a number of key points and topics covered in this review relevant to the application of algae in sustainable agriculture.
Historically, where permitting, algae have been used a source of nutrients for sustaining indigenous or traditional agricultural practices, serving as a testament to the actual nutrient contents of algae. While both micro- and macroalgae have direct fertilizing potential (nutrients), indirect fertilizing product potential (biostimulant) and the exploitation of physiological responses via different biochemical pathways are the focus of current research. Current research is exploring how to incorporate macroalgae and microalgae as part of fertilization plans to improve the health and fertility of agricultural soils. The approach is to stimulate the internal metabolism of plants and protect crops from stress and agents causing damage in the field, strengthening cultivated plants, improving productivity, and optimizing agricultural yields. Also notable is how microalgae can be used to improve soil quality and protection, including the maintenance of soil organic matter.
Though macroalgae have historically dominated algae applications in agriculture due to ease of harvest and preparation (of fertilizers or extracts), microalgae have a number of advantages for large-scale production and application as biofertilizers, in part because their production is decoupled from marine waters and can be linked with other industrial processes. Nonetheless, microalgae production for agriculture or industrial applications is hampered by technological hurdles (harvesting, among others) and sufficient market value.
What has been highlighted is the positioning of microalgae for the production of biostimulants, use as biofertilizers, and potential for alleviating stress. Their contents of active biochemical or inorganic compounds which intervene in plant growth — particularly hormones but also other compounds such as antioxidants, micronutrients, or nutrient supplements — are now of high value in the fertilizing product market.
The use of biofertilizers is rapidly gaining ground in agriculture throughout the world, offering alternatives or products which are complementary to chemical fertilizers, with the aim of maintaining agricultural production and soil fertility while reducing soil degradation and environmental contamination. The beneficial effects of algae and particularly microalgae have been documented, although the prospects for large-scale production and the feasibility of producing inexpensive formulations require more attention. New initiatives should address production methods and applications to increase the cost–benefit ratios and improve market acceptance.
Change history
17 October 2022
A Correction to this paper has been published: https://doi.org/10.1007/s42729-022-01037-x
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Kholssi, R., Lougraimzi, H., Grina, F. et al. Green Agriculture: a Review of the Application of Micro- and Macroalgae and Their Impact on Crop Production on Soil Quality. J Soil Sci Plant Nutr 22, 4627–4641 (2022). https://doi.org/10.1007/s42729-022-00944-3
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DOI: https://doi.org/10.1007/s42729-022-00944-3