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Rojas-Sánchez, B.;  Guzmán-Guzmán, P.;  Morales-Cedeño, L.R.;  Orozco-Mosqueda, M.D.C.;  Saucedo-Martínez, B.C.;  Sánchez-Yáñez, J.M.;  Fadiji, A.E.;  Babalola, O.O.;  Glick, B.R.;  Santoyo, G. Bioencapsulation of Microbial Inoculants. Encyclopedia. Available online: (accessed on 21 June 2024).
Rojas-Sánchez B,  Guzmán-Guzmán P,  Morales-Cedeño LR,  Orozco-Mosqueda MDC,  Saucedo-Martínez BC,  Sánchez-Yáñez JM, et al. Bioencapsulation of Microbial Inoculants. Encyclopedia. Available at: Accessed June 21, 2024.
Rojas-Sánchez, Blanca, Paulina Guzmán-Guzmán, Luzmaria R. Morales-Cedeño, Ma. Del Carmen Orozco-Mosqueda, Blanca C. Saucedo-Martínez, Juan M. Sánchez-Yáñez, Ayomide Emmanuel Fadiji, Olubukola Oluranti Babalola, Bernard R. Glick, Gustavo Santoyo. "Bioencapsulation of Microbial Inoculants" Encyclopedia, (accessed June 21, 2024).
Rojas-Sánchez, B.,  Guzmán-Guzmán, P.,  Morales-Cedeño, L.R.,  Orozco-Mosqueda, M.D.C.,  Saucedo-Martínez, B.C.,  Sánchez-Yáñez, J.M.,  Fadiji, A.E.,  Babalola, O.O.,  Glick, B.R., & Santoyo, G. (2022, September 19). Bioencapsulation of Microbial Inoculants. In Encyclopedia.
Rojas-Sánchez, Blanca, et al. "Bioencapsulation of Microbial Inoculants." Encyclopedia. Web. 19 September, 2022.
Bioencapsulation of Microbial Inoculants

The role of inoculants, such as plant growth-promoting fungi (PGPF) and plant growth-promoting bacteria (PGPB), on plants is to improve plant growth, production and resistance against several phytopathogens. These microorganisms are used as different types of formulations, prepared accordingly to the desired function or effect of the microorganism to be used. 

bioinoculants beneficial fungi microbial bioencapsulation

1. Introduction

The continuous increase in the world population is accompanied by a high demand for agricultural products that must be satisfied in quantity and quality. In recent decades, and particularly since the advent of the green revolution, excessive use of chemical fertilizers has taken place to maximize production and improve the quality of crops and try to increase the productivity of nutritionally poor soils [1]. However, the benefits initially observed by the use of agrochemicals on crop productivity have been overshadowed by studies that show the adverse effects of excessive use of these products on the environment [2].
Among the damages caused to the soil are the deterioration in its structure and texture and a reduction in the populations of microflora and microfauna, which together trigger a nutritional imbalance within the soil. In addition, chemical inputs are the main source of contamination in soils used for agricultural production; they contribute significantly to the contamination of water and the atmosphere, triggering diseases in living beings [2].
In addition to the above, it has been shown that the use of chemical fertilizers by plants is inefficient, since they only take advantage of ~50% or less of the chemical doses applied, regardless of the nitrogen source with which they are formulated [3], causing an accumulation of the products used in the soil.
The damages that have been caused over time by the excessive use of agrochemicals require the development and implementation of technologies that have a minimal impact on the environment and that are designed in such a way that they can maintain and preserve the productivity of the soil. In addition, agricultural products intended for human consumption that are free of chemicals gives added value to these products [4].
One of the technological options to decrease the amount of chemicals in the soil environment is to use beneficial microorganisms that can promote plant growth and reduce synthetic fertilizers without negatively affecting crop productivity [5][6]. The use of these microorganisms, also known as biofertilizers, is one of the most important contributions of biotechnology and microbiology to modern agriculture, and it is an alternative for the reduction in production costs and the environmental impact caused by the excessive use of agrochemicals [7][8].

2. The Role of Beneficial Microorganisms as Inoculants

The interaction of plants with microbial communities results from co-evolution over millions of years, contributing to the adaptation of plants on earth [9]. The interactions between microorganisms and plants occurs mainly in the portion of the soil that is in close contact with the plant root, known as the rhizosphere. This zone is defined as the volume of soil associated with and influenced by plant roots [10], constituting a favorable environment for the development of microorganisms in quantities that are much higher than those found in the rest of the soil. These high microorganism concentrations are a consequence of the fact that plants provide the necessary nutrients for the development of these microorganisms, which in turn provide the plants with substances that promote their growth, establishing a mutualistic relationship between both organisms [11].
The interactions between plants and beneficial microorganisms have been the subject of various scientific investigations, since this relationship provides a viable alternative for sustainable plant development and the conservation of the environment [4]. Some microorganisms that promote plant growth include mycorrhizal fungi, beneficial fungi or promoters of plant growth and certain rhizobacteria [12][13][14].
Mycorrhizal fungi are a group of root biotrophs that exchange mutual benefits with approximately 80% of plants and include arbuscular mycorrhizae and ectomycorrhizae from multiple fungal clades, such as Glomeromycota, Ascomycota and Basidiomycota [15]. Among the benefits of this mutualism is the supply of soil nutrients to plants in exchange for carbon from the host plants. This relationship results in an increase in the absorption of nutrients, the production of bioactive compounds and an increase in the production of fruits and tubers. In addition, this relationship has been highly effective as a nematicide, in addition to increasing the uptake of water to plants in certain environmental conditions [15][16].
Beneficial fungi or plant growth-promoting fungi (PGPF) have taken on great importance since it has been proven that they promote plant growth and, in turn, control numerous foliar and root pathogens by activating induced systemic resistance (ISR) in the host plant through various signaling pathways [8][17]. This group of organisms includes species of genera, such as Trichoderma, Aspergillus and Phoma [18][19].
Plant growth-promoting bacteria (PGPB) are a set of bacteria that inhabit the rhizosphere. Through different mechanisms, they promote plant growth and provide them with tolerance to both biotic and abiotic stress conditions [20]. Within this group it can be found species belonging to the genera Azospirillum, Azotobacter, Bacillus, Burkholderia, Enterobacter, Klebsiella and Pseudomonas, as well as some endophytic species, such as Axoarcus, Gluconacetobacter and Herbaspirillum [21][22][23].
The role of inoculants, such as PGPF and PGPB, on plants is to improve plant growth, production and resistance against several phytopathogens. These microorganisms are used as different types of formulations, prepared accordingly to the desired function or effect of the microorganism to be used. These formulations contain live or latent microorganisms (bacteria or fungi, alone or in combination) and, depending on the mechanism they use to promote plant growth (direct, indirect or both), are classified into one of three categories, i.e., biofertilizers, biostimulants or biopesticides [4][24]. The mechanisms of action of beneficial microorganisms are discussed in the next section.
Biofertilizers are formulations with one or several microorganisms that provide and improve the bioavailability of nutrients when applied to crops, biostimulants include microorganisms that promote plant growth directly through the production of hormones and biopesticides include microorganisms that are used to control phytopathogenic agents [25][26][27].

3. Mechanisms of Action of Beneficial Microorganisms

Certain microorganisms can promote plant growth through direct mechanisms or indirect mechanisms, although some mechanisms can work both directly and indirectly [28]. These mechanisms of action are briefly described below. It is recommended the reader to other excellent recent reviews in this area [29][30].

3.1. Direct Mechanisms of Action

Direct mechanisms refer to the promotion of plant growth in two ways: microorganisms make it easier for plants to acquire the nutrients they need or they help to modulate the levels of plant hormones involved in the development and growth of plants [31][32][33].
With the increased use of chemicals in agriculture, much of the nutrients, such as soluble inorganic phosphorus used as a chemical fertilizer, becomes immobilized soon after its application, making it unavailable to plants [34]. Naturally, in the soil, insoluble phosphorus is found as apatite or in some organic forms, such as inositol phosphate (phytate), phosphomonoesters and phosphodiesters [35], forms which plants cannot directly assimilate. However, some microorganisms are capable of solubilizing inorganic phosphates through the production of low molecular weight organic acids that act on the inorganic phosphates making them available so that they can be used by plants [34]. Other microorganisms contain enzymes that can break down organic phosphates into a plant usable form [32].
Another important nutrient for plants is iron. The predominant form of iron in nature is Fe2+, which is not assimilable by plants. Some microorganisms can synthesize complex peptide molecules with a high affinity for Fe3+; these peptides are known as siderophores. The siderophores trap iron forming a complex; this complex may be taken up by membrane receptors of microorganisms and thus facilitates its acquisition. These iron–siderophore complexes can also be assimilated by plants and subsequently broken down inside of the plant, thus providing plants with the iron they need [36].
Nitrogen is one of the nutrients that plants require in larger concentrations, and it is found primarily in organic form in the soil. Nonetheless, plants take up inorganic nitrogen as ammonium and nitrates, rather than the organic form; thus, nitrogen mineralization from organic to inorganic form is crucial for plant growth and crop production [37][38]. Nitrogen fixing bacteria have gained attention in this regard, due to their capability to convert atmospheric nitrogen (N2) into ammonia (NH3), which plants can use, in a process called biological nitrogen fixation. Bacteria capable of such conversion encode the enzyme nitrogenase (a highly conserved enzyme complex), which catalyzes the conversion of N2 to NH3 [39][40][41].
Biological mechanisms, such as nitrogen, sulfur or phosphorous fixation [42], production of siderophores to increase iron bioavailability [43][44], phosphate and sulfates solubilization [45][46] and iron sequestration [32] help to incorporate or increase nutrients in the soil, along with their bioavailability to the plants. This increased provision of nutrients is provided by the following organisms: Rhizobium spp., Sinorhizobium spp., Mesorhizobium spp., Azotobacter spp., Azospirillum spp., Pseudomonas spp., Bacillus spp., Aureobasidium pullulans, Epicoccum nigrum, Scolecobasidium constrictum, Myrothecium cinctum and Acidianus spp., among others [42][43][45][46].
Some rhizospheric and endophytic microorganisms can produce plant hormones or induce their synthesis in plants. Many soil bacteria can produce hormones, such as cytokinins, gibberellins or auxins. In addition, some rhizosphere microorganisms produce the enzyme 1-aminocyclopropane-1-carboxylate (ACC) deaminase, where ACC is the immediate precursor of ethylene, a hormone related to the senescence of plants and the ripening of fruits and that very high levels of this hormone inhibit plant growth. The enzyme ACC deaminase converts ACC into α-ketobutyrate and ammonia, thus ethylene is no longer produced, and ammonia and α-ketobutyrate are compounds that can be assimilated by plants [41][47][48]. ACC deaminase production has been observed in plant beneficial organisms, such as B. subtilis, P. fluorescens, B. amyloliquefaciens, Enterobacter cloacae and Trichoderma sp., among others [49][50][51].

3.2. Indirect Mechanisms of Action

Other microorganisms can promote plant growth indirectly. A common indirect mechanism is competition for space and nutrients, where the beneficial microorganism competes with a pathogen and the one with the greatest capacity to take up nutrients and the fastest growth rate proliferating in the soil displaces the pathogen and prevents it from colonizing and infecting plants [33][52][53]. The successful competition of PGPB with pathogens provides plants with a greater opportunity to grow and develop. It is worth mentioning that the production of siderophores can also be classified as an indirect mechanism, since the microorganisms with the capacity to produce these molecules and take up siderophore–iron complexes will limit the growth of the pathogen competing for this nutrient [44][54][55].
The production of antibiotics or antimicrobial compounds is a common and often studied indirect mechanism of plant growth promotion. For example, pyrrolnitrin produced by Pseudomanas spp. [56], iturine produced by Bacillus spp. [57] and syringomycin, produced by P. syringae [58] are some of the most common antipathogen antibiotics.
In addition to antibiotics, various microorganisms produce volatile organic compounds (VOCs) that can also be toxic to pathogens, preventing their growth or leading to their death, such as dimethyl disulfide produced by Bacillus sp. E25 [59] and B. thuringiensis CR71 [60]. Some of these VOCs, in addition to having antimicrobial action, can also promote plant growth directly, as is the case of dimethyl-hexa-decylamine [61]. Therefore, the production of VOCs can be classified as both a direct and an indirect mechanism.
Another indirect mechanism of plant growth promotion is the production of lytic enzymes related to the ability of the microorganism to parasitize and destroy the pathogen, as is the case of mycoparasitism carried out by fungi of the genus Trichoderma, adhering to the hyphae of the pathogen, where it secretes enzymes that degrade the cell wall, resulting in the death of the pathogen, or the destruction of its structure, preventing its development [49][62][63][64].
Finally, induced systemic resistance, initiated by the PGPB, is an indirect mechanism that involves activating the biochemical and molecular defense responses of the host plant, these may include the production of reactive oxygen species (ROS), phytoalexins, synthesis of proteins related to pathogenesis (PR), lignin accumulation at the site of infection, among others [65]. Some microorganisms that promote plant growth induce this defense response, preventing the colonization or the development of infection by phytopathogens [44][66][67].

4. Formulation of Microbial Inoculants

To enable plant growth-promoting microorganisms to be used and applied in agricultural practices, it is necessary to develop formulations based on these bioinoculants. Formulating a bioinoculant includes the entire series of procedures and technologies after the growth in culture of the microorganisms that promote plant growth. Bioinoculant formulation includes the mixture of a selected beneficial strain with a suitable vehicle that preserves the viability of the microorganism in either a dormant or metabolically active state during transport, storage and application [68]. To obtain a successful formulation, the microorganism must overcome the conditions of temperature, humidity, salinity, UV radiation and water stress present in the soil and during its formulation, in addition to being effective and competitive against the native microbial populations of the soil [1][69].
The compatibility of the physical form of the bioinoculant (solids in the form of powder, granules or capsules and liquids) and its incorporation through agricultural practices is a key factor determining the durability of the product and its ability to colonize plant roots [70]. According to the physical form of the inoculant, it is classified as a liquid formulation, a solid formulation or bioencapsulated [20][70].

4.1. Liquid Formulation

Liquid formulations use culture broths or formulations based mainly on water, mineral or organic oils. Seeds and seedlings can be immersed in the inoculant before sowing or transplanting [69][71], and for the biocontrol of pathogens or physiological stimulation, they can be sprinkled on the foliage of already established plants or applied directly to the soil [72]. This formulation method is the most commonly used. It is directly applied to crops without going through other processes following fermentation; most microorganisms can survive for more than one year if the containers are kept at ~4 °C, they are easy to inoculate and their application is very practical when implemented in irrigation or sprinkler systems. Liquid formulations are relatively low cost. However, even when its efficacy has been proven, its stability during storage is often limited due to its susceptibility to contamination with other microorganisms [68][73].
Liquid formulations of different microorganisms, or even in microbial consortia, and with the use of various additives, have managed to increase yields in agricultural fields. For example, when a liquid bioinoculant based on sugar and coconut water, including Pseudomonas spp., Bacillus spp., Klebsiella spp., Aspergillus spp., and Azotobacter spp., was used to inoculate soybean plants, the result was improved nutrient solubility and increased crop yield [74].
It has also been shown that the phosphate solubilization capacity and the survival rate of Pseudomonas and Pantonea strains increases and are preserved when they are used in liquid formulations up to three months after their formulation containing diluted concentrations of phosphate buffer and nutrient broth with glycerol [75]. In addition, Camelo-Rusinque et al. [76] assessed the population dynamics of the Azotobacter chrocoocum strain AC1 in MBR culture medium under bioreactor conditions after 105 days and found that both the cell viability and the biological activity of the strain was maintained, regardless of the storage temperature. This indicates that some liquid formulations can be used for a specific time, with the organisms retaining their activity and continuing to be viable for use as bioinoculants.

4.2. Solid Formulation

Solid formulations are used widely in the agricultural industry because of the advantages they offer during storage and transportation. A simple technique used for the preparation of solid formulations is adsorption, which consists of mixing the microorganisms with a solid support, such as vermiculite, perlite, sepiolite, kaolin, diatomaceous earth, natural zeolite, peat or clay, the latter being of great interest in agriculture thanks to its ability to act as a desiccant and provide excellent storage conditions for various inocula, as it has a good ability to adsorb agents dispersed or suspended in it [77][78].
Peat is one of the supports most used worldwide in commercial crops due to its low cost. However, being a complex organic matter, different batches present great chemical variability and, consequently, it is difficult to maintain the same quality in all batches. In addition, its storage is very susceptible to humidity, which decreases the inoculum cell survival [77]. According to Rose et al. [79], it is essential to be able to quantify the number of viable cells of each microorganism per unit weight of inoculant, to determine the inoculum potential at different application doses and for field results to be properly interpreted.
In a study by Quiroz Sarmiento et al. [80], the effectiveness of peat was evaluated with the following bacteria: Serratia liquefaciens CPAC53, S. plymuthica CPPC55, P. tolaasii P61 and P. yamanorum OLsSf5, in comparison with the encapsulation of the strains using alginate beads. Following a storage period of 150 days, the results showed that the encapsulated strains maintained the highest population. The effect of both types of bioinoculants on poblano chili seedlings (Capsicum annum L.) was also evaluated. In this case, the best results were observed with the encapsulated strains [80]. This suggests that the success in using peat as a support material for solid formulations depends on the conditions in which the bioinoculum will be used and the availability of other strategies.
A common technique of solid formulation is spraying or lyophilization. This technique allows for the realization of high microbial survival rates without the need to use any support, allowing for easy inoculum storage for long periods, at room temperature, without the need for refrigeration. One of the disadvantages of lyophilization is that it is necessary to protect the cell membrane and cytoplasm against dehydration during the storage period, using a cryoprotectant, such as mannitol and microcrystalline cellulose [81]. In this way, the cells remain viable and can be used long after lyophilization, for at least a year [82].
Lyophilized microorganisms may be mixed with a solid support or used directly. For example, in the laboratory, Grzegorczyk et al. [83] studied the survival and storage stability of a strain of Trichoderma hariazum, four strains of Trichoderma atroviride and two strains of Trichoderma virens, after culture lyophilization in solid wheat straw medium with and without the addition of maltodextrin. It was observed that the strains had a higher survival capacity (except for strain T. atroviride TRS40), compared to the addition of distilled water only, and in comparison with the bioformulation containing just maltodextrin. Three months after lyophilization, the strains remained stable and most still showed cellulolytic and xylanolytic activity.
Wessman et al. [84] studied the survival of the bacterial strains P. putida KT2440 and A. chlorophenolicus A6 after lyophilization in four different formulations, including (i) sucrose, (ii) Ficoll PM400 a sucrose polymer, (iii) hydroxyethylcellulose (HEC), and (iv) hydroxypropylmethylcellulose (HPMC). The polymers were chosen to obtain a monomeric structure, such as sucrose. The results of this research indicated that a key factor to help cell survival is the ability of the added ingredients to replace water during dehydration, thereby maintaining the structure of proteins and cell membranes in a dry state. Disaccharides, such as sucrose, show this property, while polymers, such as starch-based polysaccharide, do not. Thus, some polymers can facilitate cell survival to the same extent as disaccharides provided that certain physical properties of the formulation are controlled [84].
In fact, one of the techniques that have gained great importance in recent years thanks to its advantages, is the solid formulations developed based on polymers. These polymers, in the presence of ions or changes in chemical conditions, form complex matrices so that microorganisms become immobilized and encapsulated in the matrix and are gradually released as the polymer degrades. The technique of microorganism immobilization ultimately creates barriers between the microbes and the environment, improving their bioavailability and preserving their biological stability [85].


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