Next Article in Journal
Characterization and Expression of Phospholipase D Putatively Involved in Colletotrichummusae Disease Development of Postharvest Banana Fruit
Previous Article in Journal
Metabolic Profiling of White and Green Radish Cultivars (Raphanus sativus)
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Horticulturae
Volume 8
Issue 4
10.3390/horticulturae8040311
horticulturae-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Vermicompost and Its Derivatives against Phytopathogenic Fungi in the Soil: A Review

by
Kasahun Gudeta
1,2,*,
Ankeet Bhagat
3,
Jatinder Mohan Julka
2,
Reshma Sinha
4,
Rachna Verma
2,
Arun Kumar
5,
Shailja Kumari
6,
Fuad Ameen
7,
Sartaj Ahmad Bhat
8,*,
Ryszard Amarowicz
9 and
Mamta Sharma
2
1
School of Applied Biology, Adama Science and Technology University, Adama P.O. Box 1888, Ethiopia
2
School of Biological and Environmental Sciences, Shoolini University of Biotechnology and Management Sciences, Solan 173229, India
3
Department of Zoology, Guru Nanak Dev University, Amritsar 143005, India
4
Department of Animal Sciences, School of Life Sciences, Central University of Himachal Pradesh, Kangra 176206, India
5
School of Biotechnology, Shoolini University of Biotechnology and Management Sciences, Solan 173229, India
6
Department of Bioscience, Career Point University, Hamirpur 176041, India
7
Department of Botany and Microbiology, College of Science, King Saud University, Riyadh 11451, Saudi Arabia
8
River Basin Research Center, Gifu University, Gifu 501-1193, Japan
9
Institute of Animal Reproduction and Food Research, Polish Academy of Sciences, 10-748 Olsztyn, Poland
*
Authors to whom correspondence should be addressed.
Horticulturae 2022, 8(4), 311; https://doi.org/10.3390/horticulturae8040311
Submission received: 17 February 2022 / Revised: 1 April 2022 / Accepted: 6 April 2022 / Published: 7 April 2022
Review Reports Versions Notes

Abstract

:
Synthetic chemicals, such as fertilizers and pesticides, are abundantly used in agriculture to enhance soil fertility and prevent the occurrence of diseases, respectively. Many studies have reported a negative influence of these chemicals on the soil environment. Natural sources from earthworms and their products, as a result of vermicomposting, may be considered better alternatives. The aim of this review was to reveal the source of antifungal efficiency of vermicompost and its derivatives, such as vermiwash, coelomic fluid, skin secretion of earthworms, and metabolites from decomposer bacteria in vermicompost, in order to highlight their application in agriculture. The synergistic activity of bioactive compounds present in coelomic fluid, mucus, skin secretion, and metabolites from associated bacteria (decomposer) assisted crop plants for effective action against various soil pathogenic fungi, such as Rhizoctonia solani, Alternaria solani, Aspergillus niger, A. flavus, Fusarium oxysporum, and F. graminearum. Thus, these bioactive metabolites can be recommended to suppress plant fungal diseases. Vermicompost and its derivatives should be considered for use in agricultural fields to control harmful soil fungi and increase crop productivity.

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].
Considering these fungal infections, which cause great crop loss, both vermicompost and vermiwash can be utilized as antifungal agents to minimize the harmful effects of these pathogens. The objective of this review is to summarize the source of antifungal efficiency of vermicompost and its derivatives, such as vermiwash, coelomic fluid, skin secretion of earthworms, and metabolite secretions from decomposer bacteria of vermicompost, so that farmers can use the products in agricultural fields to control harmful soil fungi and enhance crop productivity.

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).
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.
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).

5. Vermicompost: Antifungal Efficiency

Fungal diseases are usually associated with severe morbidity and mortality in plants. The extensive use of antifungal chemicals has led to the development of drug-resistant pathogens and adverse effects on environmental health [45,46]. Vermicomposting was found to have a disease-suppressive function, making it a better alternative to chemical fungicides. The composition of earthworm secretions (for instance, Lumbricin-PG from skin secretions of earthworms possess antifungal activities) associated with vermicompost are able to protect plants against fungal pathogens [20,47]. One of the antifungal effects of vermicompost is attributed to decomposer bacteria producing a symbiotic association with earthworms. You et al. (2019) [47] demonstrated that ergosterol peroxide is a bioactive metabolite derived from powdered bamboo vermicompost that considerably suppresses R. solani mycelium growth. This bioactive compound is secreted by vermicomposting bacteria using bamboo as a resource.

6. Vermiwash as Antifungal Agent

Fusarium graminearum, a well-known pathogenic fungus, has a significant impact on plant roots, reducing the quality and yield of wheat production by 20% [48]. In crops affected by fungal infection, the application of vermiwash (a liquid extract of vermicompost rich in earthworm mucus and bioactive compounds) has been shown to minimise the pathogenic effect, reducing mycelial growth [7]. Naidu et al. (2012) [49] observed that vermiwash could prevent the growth of a powdery mildew on watermelons. It was also used to control onion black mould disease caused by Aspergillus niger [50].
The extract of Eisenia fetida has been demonstrated to have a substantial antagonistic effect on F. graminearum development [48]. When earthworm mucus is applied to agricultural land, it inhibits the growth of disease-causing microbes in the soil and possesses antifungal activity to reduce fungal pathogens by 26% [48]. On the other hand, vermiwash showed only a 16% reduction in mycelium growth, indicating that the efficacy of vermiwash was much lower than that of the applied mucus [20,48,51]. Khan et al. (2015) discovered that spraying vermiwash inoculated with arbuscular mycorrhizal (AM) fungi enhanced the physicochemical parameters of soil, assisted plant growth and development by increasing nutrient availability and boosted disease resistance. AM fungus and vermiwash provided greater synergistic advantages in controlling fungal disease than any of them alone [52].
Antifungal chemicals produced by bacteria during vermicomposting may be responsible for vermiwash’s biocontrol properties. Bacillus phylotypes found in vermicompost are responsible for the fungicidal properties of vermiwash [53]. Strains of bacteria, such as Pseudomonas fluorescens Pf1 combined with Bacillus subtilis EPCO 16, play vital roles in suppressing fungal pathogens in vermicomposting. In addition, the fungal species Trichoderma asperellum TTH1 was also isolated from vermicompost and found to be more effective as a fungal biocontrol agent against sugar beet root rot than difenoconazole treatment [54]. Bacillus species are known to establish mutualistic relationships with earthworms and produce bioactive compounds against fungal pathogens in vermicompost [53]. The combined application of Bacillus amyloliquefaciens and dipotassium phosphate (DPP) was used as a decoction to suppress the mycelial growth of Alternaria solani [55].

7. Tissue Homogenate (G-90) of Earthworms: Antifungal Activity

Earthworm tissue homogenate, commonly known as G-90 or earthworm paste, is made by mincing the entire body of the earthworm [56]. The tissue homogenate comprises CF, skin secretion, and mucus, all of which contain potent bioactive chemicals that protect earthworms from fungal pathogens. Tissue homogenate from the earthworm Eudrilus eugeniae has been proven to be effective against a variety of fungal pathogens [57] (Table 4). Different species of fungal pathogens react differently against the same concentrations of earthworm paste [57]. For instance, there was a reported maximum zone of inhibition of Aspergillus flavus growth (15.00 ± 0.57 mm) at 100 µL earthworm paste, suggesting its higher inhibition efficacy at higher concentrations.
A comparative study on the antifungal efficiency of the earthworm’s paste and fluconazole through inhibition zones demonstrated equivalent or higher efficacy of the earthworm paste at 150 µL and 200 µL concentrations (Table 5). Among four species involved in the experiment (Aspergillus niger, Penicillium citrinum, A. nidulans and Cladosporium herbarum), to assess antifungal efficacy of earthworm paste in different phytopathogenic species, P. citrinum showed a higher zone of inhibition against the paste, but A. niger possessed higher resistance with a lower zone of inhibition [58].
The efficiency of the coelomic fluid and earthworm paste against the fungal pathogens indicated in Table 2, Table 3, Table 4 and Table 5 is due to the presence of bioactive compounds that evolutionarily developed in earthworms to protect them against soil pathogens [7].

8. Decomposer Bacteria of Vermicompost/Vermiwash as Antifungal Agents

Compared to chemical fungicides, the application of vermicompost in agricultural land is encouraging to control fungal plant pathogens. Bacillus subtilis had the largest range of antifungal activity among the bacteria found in vermicompost, which produce compounds that can help a plant fight off fungal infections. The volatile organic compounds secreted by B. subtilis, such as 3-methyl-3-hexanol, were extracted from cow dung vermicomposting and shown to act against the fungal pathogen Botrytis cinereal [59].
Additionally, high levels of chitinolytic bacteria, Actinobacteria, have been reported in vermicompost. Chitinolytic bacteria can catalyze fungal cell walls at the early germination stage, ultimately hindering the growth of fungal pathogens [60]. Furthermore, various Rhizobacteria species isolated from vermicompost have been shown to strongly inhibit fungal growth on beans by 50–60% [61].
The efficiency of vermicompost/vermiwash to suppress disease is also attributed to metabolites secreted from decomposer bacteria that establish a symbiotic relationship with earthworms in their gut, cast, and burrows [7]. Bioactive substances produced by Pseudomonas as metabolites have either broad-spectrum action against fungal pathogens (Phenazines C-Acelyphloroglucinols) or are species-specific [62].
Vermicompost and associated bacteria from the genera Pseudomonas, Burkholderia, Bacillus and Streptomyces are able to produce essential metabolites to suppress pathogenic fungi of plants [63]. The source of these chemicals has been reported from mutualistic bacteria involved in vermicomposting rather than from the raw materials used in the process [47] (Table 6).

9. Future Perspective

The efficiency of vermicompost and its derivatives to prevent the development of phytopathogenic fungi in agriculture is due to the synergetic effects of bioactive compounds in the coelomic fluid, mucus, skin secretion of earthworms and metabolites from decomposer bacteria involved in vermicomposting. In the future, these metabolites should be industrially produced in large amounts by culturing these bacteria in vermicomposting so that the valuable products can be commercially available in the market for farmers.

10. Conclusions

The application of vermicomposting to agricultural land increases productivity by a multifaceted impact on soil health and crops, facilitating nutrient enrichment and preventing pathogen development. Vermicompost and its derivatives, such as vermiwash, along with associated decomposer bacteria, act against fungal pathogens. The antifungal efficacy of vermicompost may be associated with bioactive compounds present in the CF, mucus, skin secretion of earthworms and metabolites secreted by decomposer bacteria. The CF of earthworms has an inherent ability to defend worms against diseases. It inhibits the growth of a variety of fungal pathogens, such as Rhizoctonia solani, Alternaria solani, Aspergillus niger, A. flavus, Fusarium oxysporum, and F. graminearum. The metabolites from vermicomposting bacteria, CF, mucus, and skin secretion synergistically combat phytopathogenic fungi. As an organic product, vermicompost and its derivatives are environmentally friendly. Thus, these products should be used to boost agricultural productivity by nutrient enrichment and reduction of plant fungal diseases. This review provides new insights into the application of vermicompost and its derivatives in agricultural fields against plant fungal infections.

Author Contributions

Conceptualization, K.G. and A.B.; methodology, J.M.J.; validation, J.M.J., A.K. and S.K.; formal analysis, R.S. and M.S.; investigation, F.A. and R.V.; writing—original draft preparation, K.G. and J.M.J.; writing—review and editing, K.G, S.A.B. and R.A.; funding acquisition, S.A.B. and R.A. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

The authors acknowledge Alah Dekema Jara, Hawassa University, Hawassa, Ethiopia.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. El-Sabagh, A.; Omar, A.; Saneoka, H.; Barutçular, C. Some of nutritive value of canola (Brassica napus L.) as affected by organic and inorganic fertilizer. In Proceedings of the 2nd ICSAE 2015, International Conference on Sustainable Agriculture and Environment, Konya, Turkey, 30 September–3 October 2015; pp. 648–653. [Google Scholar]
  2. Nadana, G.R.V.; Rajesh, C.; Kavitha, A.; Sivakumar, P.; Sridevi, G.; Palanichelvam, K. Induction of growth and defense mechanism in rice plants towards fungal pathogen by eco-friendly coelomic fluid of earthworm. Environ. Technol. Innov. 2020, 19, 101011. [Google Scholar] [CrossRef]
  3. Ansari, A.A.; Jaikishun, S. An investigation into the vermicomposting of sugarcane bagasse and rice straw and its subsequent utilization in cultivation of Phaseolus vulgaris L. in Guyana. Am.-Eurasian J. Agric. Environ. Sci. 2010, 8, 666–671. [Google Scholar]
  4. Ansari, A.A.; Pereira, M.; Jaikishun, S. Effect of Vermiwash Obtained from Different Sources (Neem, Rice Straw and Bagasse) and Standardised Hydroponics Solution on the Growth of Colocasia esculenta (Australian Poi) in Guyana. J. Exp. Agric. Int. 2015, 7, 275–283. [Google Scholar] [CrossRef]
  5. Weltzien, H.C. Biocontrol of foliar fungal diseases with compost extracts. In Microbial Ecology of Leaves; Springer: New York, NY, USA, 1991; pp. 430–450. [Google Scholar]
  6. Hoitink, H.A.J.; Stone, A.G.; Han, D.Y. Suppression of plant diseases by composts. HortScience 1997, 32, 184–187. [Google Scholar] [CrossRef]
  7. Gudeta, K.; Julka, J.M.; Kumar, A.; Bhagat, A.; Kumari, A. Vermiwash: An agent of disease and pest control in soil, a review. Heliyon 2021, 7, e06434. [Google Scholar] [CrossRef]
  8. Vaillier, J.; Cadoret, M.A.; Roch, P.; Valembois, P. Protein analysis of earthworm coelomic fluid. III. Isolation and characterization of several bacteriostatic molecules from Eisenia fetida andrei. Dev. Comp. Immunol. 1985, 9, 11–20. [Google Scholar] [CrossRef]
  9. Gupta, S.; Yadav, S. Immuno-defense strategy in earthworms: A review article. Int. J. Curr. Microbiol. Appl. Sci. 2016, 5, 1022–1035. [Google Scholar] [CrossRef] [Green Version]
  10. Aghamohammadi, Z.; Etesami, H.; Alikhani, H.A. Vermiwash allows reduced application rates of acaricidea zocyclotin for the control of two spotted spider mite, Tetranychus urticae Koch, on bean plant (Phaseolus vulgaris L.). Ecol. Eng. 2016, 93, 234–241. [Google Scholar] [CrossRef]
  11. Tripathi, Y.C.; Hazarika, P.; Pandey, B.K. Vermicomposting: An ecofriendly approach to sustainable agriculture. In Verms and Vermitechnology; APH Publishing Corporation: New Delhi, India, 2005; pp. 23–39. [Google Scholar]
  12. Mehta, C.M.; Palni, U.; Franke-Whittle, I.H.; Sharma, A.K. Compost: Its role, mechanism and impact on reducing soil-borne plant diseases. Waste Manag. 2014, 34, 607–622. [Google Scholar] [CrossRef]
  13. Oerke, E.C.; Dehne, H.W.; Schönbeck, F.; Weber, A. Crop Production and Crop Protection; Elsevier: Amsterdam, The Netherlands, 2012. [Google Scholar]
  14. Majeed, A.; Muhammad, Z.; Ullah, Z.; Ullah, R.; Ahmad, H. Late blight of potato (Phytophthora infestans) I: Fungicides application and associated challenges. Turk. Tarim Gida Bilim Teknol. Derg. 2017, 5, 261–266. [Google Scholar] [CrossRef] [Green Version]
  15. Bottalico, A. Fusarium diseases of cereals: Species complex and related mycotoxin profiles, in Europe. J. Plant Pathol. 1998, 80, 85–103. Available online: https://www.jstor.org/stable/41997909 (accessed on 5 October 2021).
  16. Viswanthan, R. Red rot of sugarcane (Colletotrichum falcatum Went). CAB Rev. 2021, 16, 23. [Google Scholar]
  17. Becker-Ritt, A.B.; Carlini, C.R. Fungitoxic and insecticidal plant polypeptides. Pept. Sci. 2012, 98, 367–384. [Google Scholar] [CrossRef] [PubMed]
  18. Alexander, B.D.; Perfect, J.R. Antifungal resistance trends towards the year 2000. Drugs 1997, 54, 657–678. [Google Scholar] [CrossRef] [PubMed]
  19. Torres-Calzada, C.; Tapia-Tussell, R.; Higuera-Ciapara, I.; Perez-Brito, D. Morphological, pathological and genetic diversity of Colletotrichum species responsible for anthracnose in papaya (Carica papaya L.). J. Invertebr. Pathol. 2013, 135, 67–79. [Google Scholar] [CrossRef]
  20. Li, W.; Li, S.; Zhong, J.; Zhu, Z.; Liu, J.; Wang, W. A novel antimicrobial peptide from skin secretions of the earthworm, Pheretima guillelmi (Michaelsen). Peptides 2011, 32, 1146–1150. [Google Scholar] [CrossRef]
  21. Massicotte, R.; Robidoux, P.Y.; Sauvé, S.; Flipo, D.; Mathiot, A.; Fournier, M.; Trottier, B. Immunotoxicological response of the earthworm Lumbricus terrestris following exposure to cement kiln dusts. Ecotoxicol. Environ. Saf. 2004, 59, 10–16. [Google Scholar] [CrossRef]
  22. Ghosh, S. Environmental pollutants, pathogens and immune system in earthworms. Environ. Sci. Pollut. Res. 2018, 25, 6196–6208. [Google Scholar] [CrossRef]
  23. Cooper, E.L.; Kvell, K.; Engelmann, P.; Nemeth, P. Still waiting for the toll? Immunol. Lett. 2006, 104, 18–28. [Google Scholar] [CrossRef]
  24. Yadav, S. Screening of Immunocompetent Coelomic Cells in Earthworms. Int. J. Sci. 2016, 5, 43–51. [Google Scholar] [CrossRef]
  25. Prakash, M.; Gunasekaran, G. Antibacterial activity of the indigenous earthworms Lampito mauritii (Kinberg) and Perionyx excavatus (Perrier). J. Integr. Complement Med. 2011, 17, 167–170. [Google Scholar]
  26. Kobayashi, H.; Ohta, N.; Umeda, M. Biology of lysenin, a protein in the coelomic fluid of the earthworm Eisenia foetida. Int. Rev. Cytol. 2004, 236, 45–99. [Google Scholar] [PubMed]
  27. Patil, R.; Biradar, M. Earthworm’s coelomic fluid: Extraction and importance. Int. J. Adv. Res. Sci. Technol. 2017, 2, 1–4. [Google Scholar]
  28. Laverack, M.S. The Physiology of Earthworms: International Series of Monographs on Pure and Applied Biology: Zoology; Elsevier: Amsterdam, The Netherlands, 2013. [Google Scholar]
  29. Bilej, M.; Procházková, P.; Šilerová, M.; Josková, R. Earthworm immunity. Invertebr. Immun. 2010, 708, 66–79. [Google Scholar] [CrossRef]
  30. Fiołka, M.J.; Czaplewska, P.; Macur, K.; Buchwald, T.; Kutkowska, J.; Paduch, R.; Urbanik-Sypniewska, T. Anti-Candida albicans effect of the protein-carbohydrate fraction obtained from the coelomic fluid of earthworm Dendrobaena veneta. PLoS ONE 2019, 14, e0212869. [Google Scholar] [CrossRef]
  31. Li, C.; Chen, M.; Li, X.; Yang, M.; Wang, Y.; Yang, X. Purification and function of two analgesic and anti-inflammatory peptides from coelomic fluid of the earthworm, Eisenia foetida. Peptides 2017, 89, 71–81. [Google Scholar] [CrossRef]
  32. Beschin, A.; Bilej, M.; Hanssens, F.; Raymakers, J.; Van Dyck, E.; Revets, H.; Timmermans, M. Identification and Cloning of a Glucan-and Lipopolysaccharide-binding Protein from Eisenia foetida Earthworm Involved in the Activation of Prophenoloxidase Cascade. J. Biol. Chem. 1998, 273, 24948–24954. [Google Scholar] [CrossRef] [Green Version]
  33. Lange, S.; Kauschke, E.; Mohrig, W.; Cooper, E.L. Biochemical characteristics of Eiseniapore, a pore-forming protein in the coelomic fluid of earthworms. Eur. J. Biochem. 1999, 262, 547–556. [Google Scholar] [CrossRef] [Green Version]
  34. Cooper, E.L.; Kauschke, E.; Cossarizza, A. Annelid humoral immunity: Cell lysis in earthworms. In Phylogenetic Perspectives on the Vertebrate Immune System; Springer: Berlin/Heidelberg, Germany, 2001; pp. 169–183. [Google Scholar]
  35. Field, S.G.; Kurtz, J.; Cooper, E.L.; Michiels, N.K. Evaluation of an innate immune reaction to parasites in earthworms. J. Invertebr. Pathol. 2004, 86, 45–49. [Google Scholar] [CrossRef]
  36. Kauschke, E.; Mohrig, W.; Cooper, E.L. Coelomic fluid proteins as basic components of innate immunity in earthworms. Eur. J. Soil Biol. 2007, 43, S110–S115. [Google Scholar] [CrossRef]
  37. Bilej, M.; De Baetselier, P.; Beschin, A. Antimicrobial defense of the earthworm. Folia Microbiol. 2000, 45, 283–300. [Google Scholar] [CrossRef] [PubMed]
  38. Pan, W.; Liu, X.; Ge, F.; Zheng, T. Reconfirmation of antimicrobial activity in the coelomic fluid of the earthworm Eisenia fetida andrei by colorimetric assay. J. Biosci. 2003, 28, 723–731. [Google Scholar] [CrossRef] [PubMed]
  39. Rajesh, C.; Rajamanikkam, K.; Vadivu, G.N.R.; Palanichelvam, K. Coelomic Fluid of Earthworm, Eudrilus Eugeniae, Inhibits the Growth of Fungal Hyphae, in Vitro. Int. J. Eng. Adv. Technol. 2019, 9, 792–796. [Google Scholar]
  40. Sethulakshmi, K.C.; Ranilakshmi, K.C.; Thomas, A.P. Antibacterial and antifungal potentialities of earthworm Eudrilus eugeniae paste and coelomic fluid. Asian J. Biol. 2018, 5, 2456–7124. [Google Scholar] [CrossRef]
  41. Ballarin, L.; Cammarata, M. (Eds.) Lessons in Immunity: From Single-Cell Organisms to Mammals; Academic Press: Cambridge, MA, USA, 2016. [Google Scholar]
  42. Plavšin, I.; Velki, M.; Ečimović, S.; Vrandečić, K.; Ćosić, J. Inhibitory effect of earthworm coelomic fluid on growth of the plant parasitic fungus Fusariumo xysporum. Eur. J. Soil Biol. 2017, 78, 1–6. [Google Scholar] [CrossRef]
  43. Ečimović, S.; Vrandečić, K.; Kujavec, M.; Žulj, M.; Ćosić, J.; Velki, M. Antifungal Activity of Earthworm Coelomic Fluid Obtained from Eisenia andrei, Dendrobaena veneta and Allolobophora chlorotica on Six Species of Phytopathogenic Fungi. Environments 2021, 8, 102. [Google Scholar] [CrossRef]
  44. Jorge-Escudero, G.; Pérez, C.A.; Friberg, H.; Söderlund, S.; Vero, S.; Garmendia, G.; Lagerlöf, J. Contribution of anecic and epigeic earthworms to biological control of Fusarium graminearum in wheat straw. Appl. Soil Ecol. 2021, 166, 103997. [Google Scholar] [CrossRef]
  45. Kinay, P.; Mansour, M.F.; Gabler, F.M.; Margosan, D.A.; Smilanick, J.L. Characterization of fungicide-resistant isolates of Penicillium digitatum collected in California. Crop Prot. 2007, 26, 647–656. [Google Scholar] [CrossRef]
  46. Pérez-García, A.; Romero, D.; De Vicente, A. Plant protection and growth stimulation by microorganisms: Biotechnological applications of Bacilli in agriculture. Curr. Opin. Biotechnol. 2011, 22, 187–193. [Google Scholar] [CrossRef]
  47. You, X.; Wakana, D.; Ishikawa, K.; Hosoe, T.; Tojo, M. Antifungal activity of compounds isolated from bamboo vermicompost against Rhizoctonia solani AG1-IB. Adv. Microbiol. 2019, 9, 957. [Google Scholar] [CrossRef] [Green Version]
  48. Akinnuoye-Adelabu, D.B.; Hatting, J.; de Villiers, C.; Terefe, T.; Bredenhand, E. Effect of red worm extracts against Fusarium root rot during wheat seedling emergence. Agron. J. 2019, 111, 2610–2618. [Google Scholar] [CrossRef]
  49. Naidu, Y.; Meon, S.; Siddiqui, Y. In vitro and in vivo evaluation of microbial-enriched compost tea on the development of powdery mildew on melon. BioControl 2012, 57, 827–836. [Google Scholar] [CrossRef]
  50. Özer, N.; Köycü, N.D. The ability of plant compost leachates to control black mold (Aspergillus niger) and to induce the accumulation of antifungal compounds in onion following seed treatment. BioControl 2006, 51, 229–243. [Google Scholar] [CrossRef]
  51. Liu, Y.Q.; Sun, Z.J.; Wang, C.; Li, S.J.; Liu, Y.Z. Purification of a novel antibacterial short peptide in earthworm Eisenia foetida. Acta Biochim. Biophys. Sin. 2004, 36, 297–302. [Google Scholar] [CrossRef] [Green Version]
  52. Khan, M.H.; Meghvansi, M.K.; Gupta, R.; Chaudhary, K.K.; Prasad, K.; Siddiqui, S.; Varma, A. Combining application of vermiwash and Arbuscular Mycorrhizal fungi for effective plant disease suppression. In Organic Amendments and Soil Suppressiveness in Plant Disease Management; Springer: Cham, Switzerland, 2015; pp. 479–493. [Google Scholar]
  53. Hong, S.W.; Lee, J.S.; Chung, K.S. Effect of enzyme producing microorganisms on the biomass of epigeic earthworms (Eisenia fetida) in vermicompost. Bioresour. Technol. 2011, 102, 6344–6347. [Google Scholar] [CrossRef]
  54. Thilagavathi, R.; Rajendran, L.; Nakkeeran, S.; Raguchander, T.; Balakrishnan, A.; Samiyappan, R. Vermicompost-based bioformulation for the management of sugarbeet root rot caused by Sclerotiumrolfsii. Arch. Phytopathol. Pflanzenschutz. 2012, 45, 2243–2250. [Google Scholar] [CrossRef]
  55. Imran, M.; Abo-Elyousr, K.A.; Mousa, M.A.; Saad, M.M. A study on the synergetic effect of Bacillus amyloliquefaciens and dipotassium phosphate on Alternaria solani causing early blight disease of tomato. Eur. J. Soil Biol. 2022, 162, 63–77. [Google Scholar] [CrossRef]
  56. Hrženjak, T.; Hrženjak, M.; Kašuba, V.; Efenberger-Marinculić, P.; Levanat, S. A new source of biologically active compounds-earthworm tissue (Eisenia foetida, Lumbricus rubelus). Comp. Biochem. Physiol. Comp. Physiol. 1992, 102, 441–447. [Google Scholar] [CrossRef]
  57. Vasanthi, K.; Chairman, K.; Singh, A.R. Antimicrobial activity of earthworm (Eudrilus eugeniae) paste. Afr. J. Environ. Sci. Technol. 2013, 7, 789–793. [Google Scholar]
  58. Senthil, V.; Sivakami, R. Evaluation of Antimicrobial Activity of Earthworm Lampito mauritii Paste against Bacteria and Fungi. Int. J. Curr. Res. Acad. Rev. 2018, 6, 40–44. [Google Scholar] [CrossRef]
  59. Mu, J.; Li, X.; Jiao, J.; Ji, G.; Wu, J.; Hu, F.; Li, H. Biocontrol potential of vermicompost through antifungal volatiles produced by indigenous bacteria. Biol. Control 2017, 112, 49–54. [Google Scholar] [CrossRef]
  60. Yasir, M.; Aslam, Z.; Kim, S.W.; Lee, S.W.; Jeon, C.O.; Chung, Y.R. Bacterial community composition and chitinase gene diversity of vermicompost with antifungal activity. Bioresour. Technol. 2009, 100, 4396–4403. [Google Scholar] [CrossRef]
  61. Kalantari, S.; Marefat, A.; Naseri, B.; Hemmati, R. Improvement of bean yield and Fusarium root rot biocontrol using mixtures of Bacillus, Pseudomonas and Rhizobium. Trop. Plant Pathol. 2018, 43, 499–505. [Google Scholar] [CrossRef]
  62. Dowling, D.N.; O’Gara, F. Metabolites of Pseudomonas involved in the biocontrol of plant disease. Trends Biotechnol. 1994, 12, 133–141. [Google Scholar] [CrossRef]
  63. Sulaiman, I.S.C.; Mohamad, A. The use of vermiwash and vermicompost extract in plant disease and pest control. In Natural Remedies for Pest, Disease and Weed Control; Academic Press: Cambridge, MA, USA, 2020; pp. 187–201. [Google Scholar]
  64. Thomashow, L.S.; Weller, D.M. Role of a phenazine antibiotic from Pseudomonas fluorescens in biological control of Gaeumannomyces graminis var. tritici. J. Bacteriol. 1988, 170, 3499–3508. [Google Scholar] [CrossRef] [Green Version]
  65. Howell, C.R.; Stipanovic, R.D. Suppression of Pythiumultimum-induced damping-off of cotton seedlings by Pseudomonas fluorescens and its antibiotic, pyoluteorin. Phytopathology 1980, 70, 712–715. [Google Scholar] [CrossRef]
  66. Shanahan, P.; O’Sullivan, D.J.; Simpson, P.; Glennon, J.D.; O’Gara, F. Isolation of 2, 4-diacetylphloroglucinol from a Fluorescent pseudomonad and investigation of physiological parameters influencing its production. Appl. Environ. Microbiol. 1992, 58, 353–358. [Google Scholar] [CrossRef] [Green Version]
Table
Table 1. Different types of earthworm coelomocytes (adopted from Patil and Biradar, 2017) [27].
Table 1. Different types of earthworm coelomocytes (adopted from Patil and Biradar, 2017) [27].
Type of CoelomocytesShapeDescriptionsFunction
Amoebocytes/granulocytes/phagocytes Horticulturae 08 00311 i001Large in size and spherical in shapeHelps in removing harmful microbes.
Mucocytes Horticulturae 08 00311 i002Elongated and its narrow end bears nucleusSecretes mucus to keep the skin hydrated for respiratory and other physiological purposes.
Circular cells Horticulturae 08 00311 i003Nucleated, circular in shapeFunctions of these cells are not known.
Chloragogen cells or yellow cells Horticulturae 08 00311 i004Vary in shapeActs as trophocytes, participates in circulation of nutrients to different cells and organs of the body.
Table
Table 2. The effect of CF of earthworms on growth rate of fungal hyphae (adopted from Rajesh et al., 2019) [39].
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 dahliae9998+ + ++
Aspergillus flavus873+ + ++
Rhizoctonia solani4634+ + ++
Fusarium oxysporum284+ + ++
MTCC: Microbial Type Culture Collection Gene Bank located in Chandigarh, India; greatly dense mycelial growth (+ + +); restricted hyphae growth (+).
Table
Table 3. Antifungal activity shown by coelomic fluid from different species of earthworms.
Table 3. Antifungal activity shown by coelomic fluid from different species of earthworms.
Earthworm’s SpeciesFungal SpeciesResultsReferences
Eudrilus eugeniaeRhizoctonia solaniReduced disease index [2]
Eisenia fetidaFusarium oxysporumReduction of fungal growth[42]
E. eugeniaeAspergillus nigerInhibited fungal growth [40]
E. eugeniaeRhizoctonia solaniInhibited fungal growth [39]
Lumbricus rubellusFusarium graminearumReduced its germination [44]
Table
Table 4. Antifungal activity of crude earthworm paste through the Disc assay method (adopted from Vasanthi et al. 2013) [57].
Table 4. Antifungal activity of crude earthworm paste through the Disc assay method (adopted from Vasanthi et al. 2013) [57].
Fungal Species Zone of Inhibition of Fungal Growth under Different Concentrations (Mean ± SD) of Earthworm’s Paste
50 µL100 µL
Aspergillus niger (NCIM-501) 11.00 ± 0.5713.33 ± 0.33
A. flavus (Local isolate) 10.33 ± 0.3315.00 ± 0.57
Penicillium notatum (Local isolate) 10.66 ± 0.3314.33 ± 0.33
Table
Table 5. Efficiency of earthworm paste against fungal pathogens (adopted from Senthil and Sivakami, 2018) [58].
Table 5. Efficiency of earthworm paste against fungal pathogens (adopted from Senthil and Sivakami, 2018) [58].
Fungal Species Concentration of Earthworm Paste and Zone of Inhibition in mm (Mean ± SE)
25 μL50 μL100 μL150 μL200 μLFucanazole 20 μL
A. niger1.2 ± 0.224.6 ± 0.728.6 ± 0.6412.8 ± 0.6411.6 ± 0.9212.4 ± 0.52
P. citrinum1.4 ± 0.404.8 ± 0.609.8 ± 0.7212.2 ± 0.7814.8 ± 0.9216.4 ± 0.49
A. nidulans2.2 ± 0.345.8 ± 0.949.6 ± 0.9813.0 ± 0.7213.8 ± 0.9214.6 ± 0.29
C. herbarium2.4 ± 0.365.8 ± 0.829.8 ± 0.7212.0 ± 0.6413.4 ± 0.9213.8 ± 0.20
Table
Table 6. Metabolites secreted by Pseudomonas acting against fungal pathogens of plants.
Table 6. Metabolites secreted by Pseudomonas acting against fungal pathogens of plants.
Fungal Disease Metabolites Pathogen References
Black root-rot of tobaccoHydrogen cyanide 2,4-2, 4 DiacetylphloroglucinolThielaviopsis basicola[62]
Take-all of wheatPhenazines C-AcelyphloroglucinolsGaeumannomyces graminis Var. tritici[64]
Pre-emergent damping-off of cotton; Sugar beetOomycin Pyoluteorin 2, 4 DiacetylphloroglucinolPythium spp. [65,66]
Tan spot of wheat PyrrolnitrinPyrenophora triticirepentis[62]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Gudeta, K.; Bhagat, A.; Julka, J.M.; Sinha, R.; Verma, R.; Kumar, A.; Kumari, S.; Ameen, F.; Bhat, S.A.; Amarowicz, R.; et al. Vermicompost and Its Derivatives against Phytopathogenic Fungi in the Soil: A Review. Horticulturae 2022, 8, 311. https://doi.org/10.3390/horticulturae8040311

AMA Style

Gudeta K, Bhagat A, Julka JM, Sinha R, Verma R, Kumar A, Kumari S, Ameen F, Bhat SA, Amarowicz R, et al. Vermicompost and Its Derivatives against Phytopathogenic Fungi in the Soil: A Review. Horticulturae. 2022; 8(4):311. https://doi.org/10.3390/horticulturae8040311

Chicago/Turabian Style

Gudeta, Kasahun, Ankeet Bhagat, Jatinder Mohan Julka, Reshma Sinha, Rachna Verma, Arun Kumar, Shailja Kumari, Fuad Ameen, Sartaj Ahmad Bhat, Ryszard Amarowicz, and et al. 2022. "Vermicompost and Its Derivatives against Phytopathogenic Fungi in the Soil: A Review" Horticulturae 8, no. 4: 311. https://doi.org/10.3390/horticulturae8040311

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop