Vermicompost and Its Derivatives against Phytopathogenic Fungi

Vermicompost and Its Derivatives against Phytopathogenic Fungi: History

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coelomic fluid
earthworm
fungal pathogen
vermiwash
vermicompost

1. Introduction

Synthetic chemicals, such as pesticides and fertilizers, are frequently used in agriculture despite their negative impact on the environment ^[1]. However, organic products can be a better choice for pest and disease management in agriculture ^[2]. The use of natural products and resources in agriculture can help to prevent soil damage, nutrient loss, and environmental degradation incurred due to the excessive application of toxic pesticides and chemical fertilizers ^[3]^[4]. Promising natural products for application in agriculture for soil fertility and reducing the biotic stress of plants caused by soil pathogens can be found in vermicompost and its derivatives due to the bioactive compounds and metabolites from earthworms and decomposer bacteria ^[5]^[6]^[7].

Vermicompost, a natural product obtained after decomposition of organic matter by the activity of earthworms, contribute to valuable bioavailable nutrients and use full microbes to increase soil fertility. The application of vermicompost in agriculture has resulted in remarkable improvements in crop yield as well as in crop health and nutritive qualities; it increases the soil mineral content, which enhances the survival of valuable microbes ^[5]^[6]. Furthermore, vermicompost possesses antifungal and insecticidal properties by virtue of the coelomic fluid (CF) of earthworms and other bioactive compounds, making it equally effective in controlling pests and suppressing diseases ^[7]. CF is released through the dorsal pores in the form of mucus, which acts as a defense mechanism due to its antimicrobial properties ^[2]. Bioactive compounds are synthesized by various chains of amino acids to make them distinct to fight against specific pathogen, and were developed through an evolutionary process enabling earthworms to defend against soil pathogens ^[7]^[8]^[9].

Vermiwash is an important vermicompost derivative that becomes easily bioavailable to the roots of plants. It is a solution collected after draining vermicompost rich in earthworms. It contains plenty of CF and other bioactive compounds, such as enzymes, hormones, vitamins, mucus, proteins, micro- and macronutrients, and decomposer microbes, establishing a symbiotic relationship with earthworms ^[2]^[7]^[10]^[11]. The decomposer microbes in vermicompost/vermiwash release important metabolites to prevent plant diseases ^[3]^[7]^[12].

Every year, agriculture faces severe crop loss due to plant diseases. Approximate annual worldwide production tonnage lost in the 21st century has been caused by animal pests (18%), bacterial diseases (16%), and weeds (34%), resulting in an average annual loss in crop production of 68% ^[13]. The Great Irish famine in 1845-49 was the result of failure of potato crops due to late blight disease caused by Phytophthora infestans ^[14]. Similarly, various fungal pathogens are destroying major crops all over the world; for example, Fusarium spp. cause root rot in wheat ^[15], while infection by Colletotrichum falcatum results in red rot in sugarcane ^[16]. An approximately 80% reduction in rice yield has been recorded due to fungal pathogens ^[17]. As a postharvest fungal disease, anthracnose causes the spoilage of vegetables, and fruits ^[18]^[19].

2. Protective Mechanisms of Earthworm against Diseases

Earthworms live in a complex soil ecosystem where many decomposer bacteria are present in the drilosphere (soil containing earthworm secretions, burrow and cast), and these bacterial species help them to break down organic materials derived from plants and animals ^[20]. In addition, these decomposer bacteria establish symbiotic relationships with the worms in the drilosphere and in their gut to protect them from pathogenic microbes ^[7]. Earthworms are also able to protect themselves from pathogenic microbes by virtue of the bioactive compounds found in their CF, mucus and other cutaneous secretions ^[21]. Earthworm defense mechanisms include both humoral and cellular immune responses ^[22]. Chloragocytes, eleocytes, coelomocytes, granulocytes, natural killer (NK) cells and natural killer-like (NK-like) cells make up the cellular immune system of earthworms ^[23], while antimicrobial peptides, cytokines and proteins, which aid in phagocytosis, clotting, encapsulation, lysis, and agglutination, comprise the humoral immune system ^[7]^[24].

Coelomocytes are responsible for controlling the immune response of earthworms to numerous irritants in the soil ecosystem ^[24]. Essential bioactive compounds that are extracted from skin secretions, CF, and mucus of earthworms act as a humoral immune system by lysing cells of pathogenic microbes ^[22]^[25]^[26]. These compounds are important for earthworm survival and protection against pathogens and other stimuli in their surroundings.

3. Coelomic Fluid: Secretion and Biology

Earthworms belong to the phylum Annelida. Their body cavity is a “true coelom”, located between the gastrointestinal tract and the epidermis lined by the coelomic epithelium. Intersegmental septa separate the coelom into tiny compartments, which are filled with CF ^[27]. The earthworm’s body contains a significant amount of liquid, which accounts for approximately 85% of its total weight, with CF being a major component ^[28]. CF is a yellowish-colored alkaline biofluid composed of a watery matrix, plasma, specific proteins, enzymes, salts, and at least four coelomocytes, namely, amoebocytes, mucocytes, circular cells, and chloragogen cells ^[27]^[29] (Table 1).

Table 1. Different types of earthworm coelomocytes (adopted from Patil and Biradar, 2017) ^[27].

Type of Coelomocytes	Descriptions	Function
Amoebocytes/granulocytes/phagocytes	Large in size and spherical in shape	Helps in removing harmful microbes.
Mucocytes	Elongated and its narrow end bears nucleus	Secretes mucus to keep the skin hydrated for respiratory and other physiological purposes.
Circular cells	Nucleated, circular in shape	Functions of these cells are not known.
Chloragogen cells or yellow cells	Vary in shape	Acts as trophocytes, participates in circulation of nutrients to different cells and organs of the body.

In addition to coelomocyte cells, CF contains many enzymes, such as proteases, metalloenzymes, lysozyme, fibrinolytic enzymes, antimicrobial proteins, and polysaccharides ^[30]. They have agglutinating, proteolytic, hemolytic, mitogenic, anti-pyritic, tumoratic, and antibacterial capabilities, among other biological activities ^[31]. In general, innate immunity based on coelomocytes and other components of CF (variety of bioactive components) helps to combat pathogenic microbes ^[32]^[33]^[34]^[35]. Foreign material is recognized by lectin glycoproteins present on the cell surface, resulting in agglutination and lysis ^[36].

CF is transported between adjacent segments via sphincter-lined channels within each septum. Each compartment of the coelomic cavity has paired nephridia and a single dorsal pore through which CF is ejected when the worm is irritated or while they are moving to moisten and lubricate their burrow, subsequently making CF a component of vermicompost/vermiwash ^[7]^[37]^[38]. CF is important in maintaining homoeostasis and locomotion, acting as a humoral immune factor and promoting communication between the inner and outer environments of earthworms ^[34].

4. Antifungal Activities of Coelomic Fluid and Skin Secretion of Earthworms

Individual components of CF have also been shown to inhibit fungal growth in vitro ^[39]. Lumbricin-PG is a bioactive compound derived from the skin secretion of the earthworm Pheretima guillelmi. It contains 59 amino acid residues with antibacterial and antifungal properties ^[20]. In vermicompost/vermiwash, these bioactive substances have a crucial role in suppressing fungal diseases of plants ^[40]. Another CF component, lysenin, with a size of 33 kDa, is a pore-forming protein recovered from Eisenia fetida, which has been shown to play a defensive role against bacterial and fungal infections ^[41]. Rajesh et al. (2019) ^[39] reported a reduction in fungal growth on petri dishes when treated with CF.

In another experiment performed by Rajesh et al. (2019) ^[39], CF from Eudrilus eugeniae was shown to effectively inhibit the growth of four different pathogenic fungal species (Table 2). Therefore, in the control group where no coelomic fluid was applied, the fungal growth was higher than that in the experiment where the presence of coelomic fluid greatly reduced the growth of fungal pathogens.

Table 2. The effect of CF of earthworms on growth rate of fungal hyphae (adopted from Rajesh et al., 2019) ^[39].

Fungal Species	MTCC Number	Growth in Control	Growth with Coelomocytes
Verticillium dahliae	9998	+ + +	+
Aspergillus flavus	873	+ + +	+
Rhizoctonia solani	4634	+ + +	+
Fusarium oxysporum	284	+ + +	+

MTCC: Microbial Type Culture Collection Gene Bank located in Chandigarh, India; greatly dense mycelial growth (+ + +); restricted hyphae growth (+).

Similarly, coelomocytes of the earthworms Dendrobaena veneta and Eisenia fetida inhibited the growth of the plant-parasitic fungus Fusarium oxysporum after 48 or 72 h of treatment ^[42]. Sethulakshmi et al. (2018) ^[40] reported the antifungal efficacy of CF from Eudrilus eugeniae against Aspergillus niger and Candida albicans, with the highest inhibitory areas of 16 mm and 18 mm, respectively. Delayed germination of the fungal spores may also account for the antifungal efficacy of CF ^[39].

The CF of different species of earthworm displays different anti-fungal activities ^[43]. Researchers have evaluated the effects of coelomic fluid of three species of earthworms (Allolobophora chlorotica, Dendrobaena veneta, and Eisenia andrei) against six species of phytopathogenic fungi, including Fusarium culmorum, Berkeleyomyces basicola, Rhizoctonia solani, Globisporangium irregulare, Sclerotinia sclerotiorum, and Macrophomina phaseolina. The inhibitory effect of the coelomic fluid of Eisenia andrei against Rhizoctonia solani was higher than that of other earthworm species ^[43].

In 2020, Nadana et al. ^[2] performed an experiment on detached leaves of rice plants treated with CF and agar blocks containing Rhizoctonia solani. In the experiment, CF-treated leaves showed no signs of necrosis even after inoculation with R. solani, while the necrosis spots appeared on untreated leaves. At seven days of post inoculation, the disease index ranged between 25% and 50% in rice leaves treated with CF; in contrast, it ranged between 75% and 100% in control leaves not treated with CF. This experiment suggested that CF can prevent rice plants against fungal pathogens. Other research also confirmed that coelomic fluid from different species of earthworms effectively reduced growth of fungal pathogens (Table 3).

Table 3. Antifungal activity shown by coelomic fluid from different species of earthworms.

Earthworm’s Species	Fungal Species	Results	References
Eudrilus eugeniae	Rhizoctonia solani	Reduced disease index	^[2]
Eisenia fetida	Fusarium oxysporum	Reduction of fungal growth	^[42]
E. eugeniae	Aspergillus niger	Inhibited fungal growth	^[40]
E. eugeniae	Rhizoctonia solani	Inhibited fungal growth	^[39]
Lumbricus rubellus	Fusarium graminearum	Reduced its germination	^[44]

This entry is adapted from the peer-reviewed paper 10.3390/horticulturae8040311

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