Cyanobacterial strain metabolites [10].
Abstract
Cyanobacteria are photosynthetic prokaryotes that can be considered as a promising source for environment-friendly sustainable agriculture. Various species of cyanobacteria have been described as biofertilizers and plant biostimulants. They can affect nutrient utilization efficiency, plant growth, gene expression, and the quality and quantity characteristics of the phytochemical composition of plants by producing many highly effective chemical compounds such as enzymes and hormones. Cyanobacteria can also induce plant resistance against biotic and non-biotic stresses. They increase plant tolerance through their direct effect on the soil or by induction of activation of plant reactions. Cyanobacteria can reduce the effect of salinity by producing extracellular polysaccharides or compatible solutions, and increase germination in drought conditions. Cyanobacteria activate plant defense responses to control plant pathogens as the inducer of systemic plant resistance against pathogens, and also, they are an effective strategy as a biocide against bacteria, fungi, and nematodes that attack plants.
Keywords
- cyanobacteria
- sustainable agriculture
- biostimulants
- biofertilizer
- bioactive compound
- phytohormones
1. Introduction
Conventional agriculture involves large-scale use of synthetic fertilizers, and pesticides to increase food production and address the needs of a rapidly growing population. However, this approach has hurt soil microbes, resulting in a reduction of agricultural output. As an alternative, sustainable agriculture focuses on addressing societal concerns about food quality and environmental protection through better management practices. One such practice is using microbial fertilizers as plant growth promoters to improve yields. Cyanobacteria are a type of plant growth-promoting microbes (PGPMs) that are commonly used in sustainable agriculture [1, 2]. These prokaryotic photoautotrophic microorganisms, some of which are facultative heterotrophs, can thrive in various environments, even in extreme conditions [3]. Cyanobacteria can be biofertilizers to solubilize phosphate, improve soil structure and nutrient uptake, and reduce soil salinity. They are also capable of increasing soil nitrogen content through nitrogen fixation from the atmosphere, making them a valuable addition to biofertilizers [4]. Additionally, cyanobacteria produce bioactive molecules like phytohormones, polysaccharides, phenolic compounds, and amino acids that can serve as high-quality biostimulants, promoting plant growth and improving physiological functions. These metabolites also play a vital role in protecting plants against abiotic stresses and helping them fight against pests and pathogens.
2. Cyanobacterial biofertilizer
Cyanobacteria are one of the most important groups of microorganisms that are used as biofertilizers in sustainable agriculture. The common reasons for using cyanobacteria as biofertilizers are their ability for nitrogen fixation, soil amendment, and solubilization of phosphate in the soil.
2.1 Nitrogen fixation by cyanobacteria
In intensive agriculture, nitrogen (N) supplementation is done through the application of N-rich fertilizers such as urea and ammonium sulfate to the soil. However, 50% of nitrogen is lost to the environment due to ammonia volatilization, denitrification, leaching, and surface runoff, and only 50% of N is absorbed by the plant, and this is the major drawback of the mentioned method. To solve this problem, the lack of soil nitrogen content can be corrected by fixing atmospheric nitrogen. Atmospheric nitrogen (N2), the most abundant source of nitrogen in the earth, is very stable because of the triple bond between the nitrogen atoms; almost inert N2 can be chemically reduced to NH3, but it is only possible at very high temperatures and high pressures of N2 and H2 (Haber-Bosch process). Therefore, in order to increase uptake by plants, this process requires high energy to reduce N2 to ammonia [5, 6].
Atmospheric nitrogen fixation is one of the most important functions of cyanobacteria, which are used as biofertilizers. As the main nitrogen-fixing agents in agricultural soils, they fix atmospheric nitrogen and are then re-assimilated by higher plants [6, 7]. Importantly, cyanobacteria fix N2 at ambient pressure and temperature; however, it is still an energetically expensive process for N2-fixing organisms. Nitrogenase requires 16 ATP and 8 low potential electrons to reduce N2 to NH3 (usually provided as reduced ferredoxin) [5]. Nitrogenase is inactivated by oxygen, so oxygenic photosynthesis and nitrogen fixation processes are incompatible [8].
To solve the problem, two different mechanisms have evolved to separate two processes: First process is temporal separation (day-night rhythm): Nitrogen, accumulated during the day by stored glycogen granules in the form of a nitrogen-rich polymer (cyanophycin), is fixed at night [9, 10]. Another process is spatial separation (cell differentiation). Some cyanobacteria, such as
Heterocyst-based N2 fixation is the most dominant and common mechanism in cyanobacteria. This process can occur as a symbiotic relationship between cyanobacterial species and the host plant in which the microorganisms colonize the leaves and roots of the host plant [12]. In plant leaves, cyanobacteria first enter the tissue through the stomata and then colonize the intercellular spaces by forming a cyanobacterial ring; while in the roots, loose and strong colonies are formed on root hairs and root surfaces, respectively [6, 13]. Larger and rounder shapes, thicker cell walls, and accumulation of cyanophycin granules at the border with neighboring cells distinguish heterocysts from vegetative cells [10, 14]. The schematic of nitrogen fixation in heterocysts of cyanobacteria is shown in Figure 1.
2.2 Phosphorus uptake by cyanobacteria
Phosphorus, as an essential mineral for plant growth and development, is the limiting nutrient for biomass production in agriculture, its availability in the highest amount (after nitrogen) is required for plant growth and yield, and it plays a key role in storing and using energy by soil microorganisms. However, plants or microbes are likely to be challenged to obtain phosphorus from the soil in order to grow, because a large part of soil organic phosphorus becomes inaccessible through fixation or adsorption to clay soil particles [15] and also, phosphorus is forced into relatively inaccessible inorganic pools as a result of mineral phase precipitation reactions with calcium and magnesium in alkaline soils, and iron and aluminum in acidic soils. Therefore, phosphate fertilizers are often added to the soil [16].
To release phosphate from inorganic and organic pools of total soil phosphorus, cyanobacteria, as specific phosphate-solubilizing microorganisms, are used [17]. Cyanobacteria probably solubilize phosphate by two mechanisms. First is the release of organic acids which can solubilize phosphorus [18], and the second mechanism is to synthesize a calcium ions (Ca2+) chelator which directs the dissolution in the correct direction without changing the pH of the growth medium [19]. The important role of cyanobacteria in mobilization of inorganic phosphates is performed through extracellular phosphatases; by extracting the organic acids enzymatic profile of the soil inoculated with cyanobacteria, it was found that acid phosphatases and alkaline phosphatases are involved in phosphate solubilization, so inoculating soils with species such as
2.3 The role of cyanobacteria in saline and sodic soil amendment
Saline and sodic soils that are rich in salt and/or have an alkaline nature, also known as salt-affected soils, are typically not conducive to the growth of plants [22]. The alkaline soil is identified by its high pH, plentiful exchangeable sodium ions, elevated electrical conductivity, and substantial presence of carbonates [23]. This type of soil has restricted aeration, inadequate hydraulic conductivity, and elevated osmotic pressure, hindering plant roots and absorption of water and nutrients. The high salinity of the soil, due to increased osmotic stress and build-up of sodium and chloride ions, can negatively affect plants’ metabolic activities and growth. Moreover, salt stress can diminish the microbial population in the soil and affect carbon cycling. The high concentration of salt in these soils leads to the formation of a rugged and water-resistant layer [22, 24, 25, 26].
Cyanobacteria, in association with plants, play a crucial role in mitigating salt stress. The effective use of cyanobacteria in the remediation of agricultural soils affected by salt has been proven across a variety of soil types and weather conditions [27]. Numerous species of cyanobacteria have the ability to adapt to different salinity conditions. Cyanobacteria in the rhizosphere instigate salt tolerance in crops and protect them from salt disruption. Many studies show the enhancements in the growth and yield of key crops like wheat, maize, and rice, credited to the direct de-salinization by cyanobacteria [27, 28]. Cyanobacteria through various mechanisms improve saline and sodic soils. These encompass active ion expulsion, nitrogen fixation, synthesis of phytohormones, supply of compatible solutes, discharge of extracellular polymeric substances, and a variety of defense enzymes during the process of soil reclamation [28, 29, 30]. Cyanobacteria can increase the soil’s water retention and biomass after their death and decomposition [31]. Furthermore, some cyanobacterial species can eliminate soluble sodium from the soil
3. Cyanobacterial biostimulant
Biostimulants are a distinct compound from biofertilizer that has a direct effect on plants regardless of nutrient content, increasing crop productivity. By applying plant biostimulants on plants, natural mechanisms related to increasing plant growth, nutrient utilization efficiency, and tolerance to abiotic stress factors are stimulated [33, 34]. In the scientific community, cyanobacteria and microalgae are known as promising biological sources for the production of a new class of high-quality biostimulants, which is why today the main focus is on these microorganisms. Cyanobacteria are able to produce bioactive molecules, affecting plants even at low doses. In addition, at highly controlled cultivation conditions, biomass with more stable chemical and functional characteristics can be obtained [3]. There are various types of molecules, among biostimulants, that can be extracted from cyanobacterial cells, and they include phytohormones, polysaccharides, protein hydrolysates, and amino acids [35]. Cyanobacterial strain metabolites are presented in Table 1.
Class | Metabolites | Cyanobacterial strains |
---|---|---|
Phytohormones | Auxins, abscisic acid, cytokinins, gibberellins, ethylene | |
Phenolic compounds | Flavonoids, phenolic acids, cell wall phenolics | |
Terpenoids | Isoprene, limonene, linalool, β-phellandrene, farnesene, bisabolene | |
Carotenoids | β-Carotene, astaxanthin, zeaxanthin, canthaxanthin, lutein, lycopene, echinenone, phytoene | |
Peptides | Peptides, proteins, free amino acids | |
Polysaccharides | β-Glucans, lipopolysaccharides, chitin, carrageenan | |
Vitamins | Riboflavin, thiamine, ascorbic acid, nicotinic acid, cobalamine, phenothene, pyridoxine, folic acid |
3.1 Phytohormones
Auxin, cytokinin, gibberellic acid, ethylene, abscisic acid, salicylic acid, and jasmonic acid are examples of phytohormones known for their low molecular weight and signaling; their function is to coordinate many cellular activities in a plant cell [36]. The hormonal content of cyanobacteria and their capacity to stimulate endogenous hormone synthesis in treated plants have proven their ability to elevate plant growth. Obviously, like plant cells, some phytohormones are produced in these microorganisms [3].
3.1.1 Auxin
Auxin is a phytohormone that plays a key role in the precise control of plant growth and development; its effect on plants is well known. The main auxin in higher plants, indole acetic acid (IAA), has a structure consisting of an indole ring and an acetic acid side chain. IAA is basically a hetero-aromatic organic acid and exerts strong effects on plants; for example, it increases cell elongation, prevents or delays leaf abscission, and stimulates flowering and fruiting [36, 37]. Studies have shown that IAA produced in cyanobacterial species such as
3.1.2 Cytokinins
Cytokinins are one type of phytohormones, and their structure consists of N6-substituted adenine derivatives containing aromatic or isoprenoid side chains. They affect several plant physiological processes, such as morphogenesis, development of chloroplast, seed dormancy, leaf senescence, so they are very valuable in agriculture. Cytokinins cause cytoplasm division and are useful in reducing the adverse effects of abiotic stresses on plant growth [38, 39]. Similar to plants, the biosynthesis of cytokinins in cyanobacteria is carried out using isopentenyl transferases (IPTs); however, there are slight differences in the biosynthesis mechanism. It has been shown that the use of cyanobacterial supplements in the field has been led to the induction of adventitious roots and shoots on petiolar as well as internodal segments. According to the results of leaves, roots, and stems, explants of treated plants with cyanobacterial extract or cell suspension also showed successful regeneration [39, 40].
3.1.3 Gibberellic acid
Another phytohormone is gibberellic acid (GA3), which belongs to diterpenoid gibberellins. GA3 is a plant growth regulator; its function is to regulate plant growth and affect various developmental processes involving stem germination, elongation, flowering, and enzyme production. It has been reported that the extracellular extracts of
3.1.4 Abscisic acid
Abscisic acid (ABA) is another plant growth regulator; it is a natural sesquiterpene produced in plants and cyanobacteria. ABA inhibits growth and metabolism, improves fruit ripening and senescence, and also has remarkable effects on seed development and plant tolerance to biotic or abiotic stresses. The ability to produce this phytohormone in cyanobacteria such as
3.1.5 Ethylene
This phytohormone is a gaseous hormone and its function is to regulate developmental processes like senescence, fruit ripening, cell division and elongation, and tolerance to biotic and abiotic stresses. Ethylene synthesis has been reported in cyanobacteria such as
3.2 Polysaccharides
Cyanobacterial polysaccharides are promising plant biostimulants that can be found as cell envelope compounds, storage molecules, and extracellular polysaccharides (EPS). In general, cyanobacterial polysaccharides have three fates: to be combined with the cell wall, to be secreted as distinct structures (sheath, capsule, stalk), or to be released as mucilage [34, 46]. Maximum structural diversity and functional versatility are found in EPS; the functions of these polysaccharides, which interface with the surrounding environment, vary depending on the species, from a primary mechanism for survival in extreme environments to defense against toxins, heavy metals, predators, and other antagonists [47]. The key role of exopolysaccharides in soil aggregation is due to their gluing properties and binding to heavy metals and sodium ions, improving plant development in saline or contaminated soils [46].
Signaling pathways reliant on microbe-associated molecular patterns are common mechanisms through which the stimulatory properties of cyanobacterial polysaccharides may be explained. Soil enzymes such as β-glucanase and chitinase secreted by microorganisms can hydrolyze complex polysaccharides; then, receptors on plant membranes can recognize these neutral sugars from polysaccharides as microbial-derived compounds, providing organic carbon for the growth and development of beneficial microbes and also leading to form beneficent biofilms in the rhizosphere [6, 48]. Some ESP-producing cyanobacteria among different species of microalgae are
3.3 C-phycocyanin
Cyano-phycocyanin (CPC) is one of the cyanobacterial bioactive pigments that are usually isolated from
3.4 Phenolic compounds and amino acids
One of the most principal classes of natural antioxidants are phenolic compounds, which are found in many organisms, including cyanobacteria. There are different amounts of polyphenolics such as caffeic, gallic, vanillic, ferulic acids, flavonoids, kaempferol, and quercetin in cyanobacterial extracts. The existence of polyphenols in these microorganisms demonstrated their ability to scavenge free radicals, chelate metals, and protect themselves against oxidative damage [42, 52]. Cyanobacterial strains that contain high amounts of polyphenols will achieve better ecological adaptation under different stress conditions by producing and releasing a wide range of bioactive compounds [42, 53]. Other organic compounds for applying as plant biostimulants to aid plant growth are amino acids that are found in cyanobacteria. Some of these microorganisms, such as
4. Role of cyanobacteria in plant health
Plants can benefit from cyanobacterial metabolites in various ways, such as enhancing their resistance to biotic and abiotic stressors and improving their growth and development. These metabolites are rich in bioactive substances and secondary metabolites that act as signal molecules to stimulate plant growth and stress tolerance [55, 56].
4.1 Cyanobacteria against plant abiotic stresses
Plant growth and development are adversely affected by abiotic stresses, which include extreme temperature, water scarcity or excess, high salt concentration, heavy metal toxicity, and ultraviolet exposure [57]. Plants spend most of their energy on maintenance, and vegetative and generative growth when the environment is favorable. But when they face harsh environmental conditions (such as cold, heat, drought, and salinity), they divert their resources to cope with stress, which reduces their growth and yield [58].
Cyanobacteria use different mechanisms to reduce abiotic stress in plants, which involve biochemical and molecular mechanisms such as increasing osmotic adjustment, proline accumulation, increased glutathione level, jasmonic acid and decreasing stress-related gene expression, and enhancing stress resistance gene synthesis and expression. Low-molecular-weight osmolytes, such as glycine betaine, amino acids, organic compounds, and various enzymes, also contribute to plant growth and development under stress conditions [59, 60].
Plants exposed to abiotic stresses show less damage when they interact with cyanobacteria. This occurs through both direct and indirect functions. The direct function is the effect of cyanobacteria on the soil quality, and the indirect function is the induction of specific responses in plants by cyanobacteria [57, 60]. Plants can cope with abiotic stresses better with the help of induced systemic tolerance (IST). This involves the production of phytohormones, such as IAA, cytokinins, and abscisic acid (ABA), which enable plants to withstand harsh environmental conditions. Additionally, the synthesis of antioxidants such as superoxide dismutase (SOD), peroxidase (POD), ascorbate peroxidase (APX), catalase (CAT), and glutathione reductase (GR) also reduces the damage caused by abiotic stresses [59, 61]. Another way to enhance plant resistance to abiotic stresses is to transfer genes from cyanobacteria that participate in fatty acid biosynthesis, carbon metabolism, and pigment biosynthesis [60].
4.2 Cyanobacteria against pests and pathogens (biocontrol)
Plant pests and pathogens are agents that cause disease and can be classified as bacteria, fungi, oomycetes, viruses, nematodes, or other pests. They are widely dispersed throughout the ecosystem and have the potential to negatively impact the fruit, stem, leaves, and root systems of several crops grown in all types of cultivation, leading to significant financial losses [62]. Some plants possess defense and resistance mechanisms, such as regulating gene expression, inducing or inhibiting particular metabolic pathways, and regulating signaling pathways to produce secondary metabolites with antibacterial and antioxidant properties. To reach the high desired production, however, the use of external protective agents is essential [58].
Numerous physiologically active and/or biocidal chemicals are known to be produced by cyanobacteria. These compounds may be able to counteract various pests and diseases or stimulate systemic and local resistance in plants. This presents a desirable and different strategy that does not have the drawbacks of chemical control, which is crucial for sustainable agriculture [60].
There is ample evidence that cyanobacteria have fungicidal properties. Numerous investigations, both
Results regarding the use of cyanobacteria in the management of plant pathogenic nematodes are limited but extremely encouraging. When cyanobacteria come into touch with plant roots, they can trigger various defense mechanisms against nematodes. Similar to other pathogen families, antibiosis is the most extensively documented mechanism. It can cause nematodes to experience a variety of outcomes, including paralysis, death, accelerated egg hatching, and suppression of gall formation [60, 65].
Cyanobacteria can also be used to combat insects in agriculture. The generation of potent poisons is the primary means by which cyanobacteria fight insects. Some cyanobacteria species have the ability to trigger plant systemic resistance against insects in addition to producing poisons [60, 66].
5. Application and mode of action of cyanobacterial biostimulant
The method of application and the mechanisms by which cyanobacteria and their metabolites act as biostimulants are reviewed in this section.
5.1 Method of application
Biostimulants derived from cyanobacteria and microalgae have various forms of application, such as dry biomass, cell extracts, spent medium, or supernatant. The condition of the biostimulants determines the application method. They can be applied in different ways, such as soil drench or fertigation by irrigating the soil, seed treatments or primers for the plant seeds, and foliar spray for the leaf surface [67, 68]. Many factors influence the content and concentration of active compounds in cyanobacteria, such as species, application and extraction method, season, sampling site, culture and environmental conditions [69, 70]. The cyanobacterial bioactive metabolites may also deteriorate over long storage periods. Storage and shelf life are an important parameter that can affect root stimulation, and antioxidant and antibacterial activities of biostimulants were influenced by storage time, temperature, lighting conditions, and temperature [68, 71]. Figure 2 shows the impact of cyanobacterial bioproducts on the crop and soil.
5.2 How cyanobacterial biostimulants act?
The effects of cyanobacterial biostimulants on plants are not well understood yet. Studying these mechanisms is complex and challenging. The variety and intricacy of compounds make it difficult to identify how biostimulants work. However, biostimulants are facilitators that can influence plants directly or indirectly. Direct effects include photosynthesis enhancement, nutrient uptake improvement, gene and metabolic pathway control, and phytohormone regulation, while indirect effects involve soil microbiome alteration, soil structure amelioration, and organic matter decomposition [72, 73, 74, 75]. New methods such as omics approaches can help overcome the limitations in understanding how cyanobacterial biostimulants work [68].
6. Cyanobacteria: the effective key for space agriculture
To carry out space missions or settle in space, humans need some resources such as food, oxygen, which can be provided through space agriculture. Space agriculture means the cultivation and production of plants outside the earth [76]. Earth’s environment is different from space and other bodies; plants that grow on the Earth and have adapted to its climate cannot grow outside the planet without any difficulties. The environment of space and other planets are generally extreme and the environmental parameters such as radiation exposure, magnetic field, light intensity, and microgravity exposure are in a different range from the Earth; therefore, it is very hard for plants to tolerate them [77, 78].
Using cyanobacteria is a novel and interesting method of growing plants in space. These photosynthetic microorganisms have survived in the extreme environments of the earth such as hot springs, deep seas, polar region [79] for billions of years, they have given life to the earth by photosynthesis, and they have the ability to deal with several stresses by producing secondary metabolites. Spatial stresses can increase the production of secondary metabolites by cyanobacteria and the use of cyanobacteria that grow up at this condition subsequently may enhance the growth and yield of plants [78]. Although some studies have been conducted on space agriculture and have investigated its efficiency, there are still several challenges that should be considered [80, 81, 82]. Investigating the challenges is necessary to state with certainty that using space agriculture in space settlements is a reliable approach.
7. Conclusion
Cyanobacteria are photosynthetic prokaryotes that can enhance plant performance, resilience, and sustainability. As biofertilizers, they can solubilize phosphate, improve soil quality and nutrient availability, and lower soil salinity. They can also enrich soil nitrogen by fixing atmospheric nitrogen, making them a useful supplement to biofertilizers. Moreover, cyanobacteria produce various bioactive compounds, such as phytohormones, polysaccharides, phenolic compounds, amino acids, and others, that can stimulate plant growth and development as biostimulants. By applying them through soil drenching or foliar spray, they can help plants cope with harsh environmental conditions, such as extreme temperatures, salinity, pests, and pathogens. Cyanobacterial metabolites may also indirectly benefit plants by inducing their defense system against biotic and abiotic stresses. Cyanobacteria can make bioactive molecules that boost plant growth and health even at low doses. They can also grow in controlled systems with stable composition and effects. These features make cyanobacteria a valuable bioresource for developing new and high-quality biostimulants for eco-friendly farming.
Acknowledgments
Thanks go to Ab-O-Aftab Zist Farayand (Water & Sun Bioprocess) R&D team.
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