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De Araújo, J.V. Helminthophagous Fungi. Encyclopedia. Available online: https://encyclopedia.pub/entry/16575 (accessed on 19 May 2024).
De Araújo JV. Helminthophagous Fungi. Encyclopedia. Available at: https://encyclopedia.pub/entry/16575. Accessed May 19, 2024.
De Araújo, Jackson Victor. "Helminthophagous Fungi" Encyclopedia, https://encyclopedia.pub/entry/16575 (accessed May 19, 2024).
De Araújo, J.V. (2021, November 30). Helminthophagous Fungi. In Encyclopedia. https://encyclopedia.pub/entry/16575
De Araújo, Jackson Victor. "Helminthophagous Fungi." Encyclopedia. Web. 30 November, 2021.
Helminthophagous Fungi
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This entry is adapted from the peer-reviewed paper 10.3390/parasitologia1030018

Helminthophagous fungi can be divided into five groups: nematode-trapping/predatorial, opportunistic or ovicidal, endoparasitic, toxin-producing, and producers of special attack devices. The fungi of the first and second groups produce modified hyphae called traps, with which, by a mechanical/enzymatic process, they bind and digest nematode larvae, eggs, cysts, and nematode females. Thus, they are the ones that best act in the predation of animal parasites. Supplied orally, after passing through the gastrointestinal tract of animals, fungal structures such as conidia, mycelium, and chlamidospores germinate in the feces, forming a network of hyphae with the ability to capture and destroy infective forms of animal parasitic helminths.

nematophagous fungi predatory fungi ovicidal fungi

1. Brief History of Helminthophagous Fungi

There are many studies from across the world demonstrating the successful implementation of helminthophagous fungi for the biological control of parasites in animal production systems. It should be emphasized, a priori, that the term “helminthophagous fungi” is the best one to use due to the ability and diversified action of these organisms against not only nematodes but also cestodes and trematodes. However, the term nematophagous fungus is still the most used in the scientific literature.

Since 2014, several studies carried out on an experimental basis have proposed the efficacy of helminthophagous fungi from the predatorial group ( Duddingtonia spp. , Arthrobotrys spp. and Monacrosporium spp.) and from the ovicidal group ( Pochonia chlamydosporia and Mucor circinelloides ) against the decrease in the rates of recurrence of helminth infections in different parts of the world [1][2][3][4][5][6][7]. In these studies, successful experiments demonstrated the great versatility of helminthophagous fungi in the classic biological control of helminths.

In the last five years, commercial formulations containing D. flagrans started became commercially available. In Brazil (Bioverm ® —AC001, GhenVet Saúde Animal, Paulínia, Brazil), Australia, and New Zealand (BioWorma ® —NCIMB 30336, BioWorma, Sydney, Australia), these products are already used, with administration in animal feed [5][8][9][10][11].

1.1. Duddingtonia flagrans

The fungus D. flagrans acts as the main predatory fungus of gastrointestinal parasitic nematode larvae. Relevant results were published after using Bioverm® (GhenVet Saúde Animal, Paulínia, Brazil), a commercial product based on D. flagrans (AC001). Bioverm® is licensed by the Brazilian Ministry of Agriculture, Livestock, and Supply, and can be used to combat nematodiosis in domestic animals [5].
Duddingtonia flagrans was classified as “Old friend of researchers”, a tribute to the great diversity of action that this fungus has [12]. Over the years, a series of important studies demonstrating the effectiveness of strain AC001 in the production of extracellular enzymes and crude enzymatic extract denoted its ability to be tested against the control of helminth gastrointestinal parasites [6][13][14].

1.2. Pochonia chamydosporia

The fungus P. chlamydosporia (Goddard) Zare and Gams (syn. Verticillium chlamydosporium) parasitizes helminth eggs through specialized structures called appressoria, which allow the colonization of the egg surface and penetration by mechanical and enzymatic action [15][16]. This fungus also produces chlamydospores in abundance. Several studies have addressed the efficacy of P. chlamydosporia in the control of helminths in domestic animals such as Oxyuris equi [17], Ancylostoma ceylanicum, Ascaris suum [18], Fasciola hepatica [19][20], Toxocara canis [21], and in poultry helminths [13][22][23].
There are reports that P. chlamydosporia, in addition to ovicidal action, parasitises female phytonematodes of the genus Meloidogyne, which are colonized and completely digested [24][25]. Several secondary metabolites produced by this fungus have been described as promising to be applied as anthelmintics [26][27]. Intermediate hosts of trematodes, such as the mollusk Pseudosuccinea columella, also have their offspring affected by this fungus [28].

1.3. Mucor circinelloides

Another species capable of adhering to the surface of the eggs of certain helminths, penetrating and feeding on their contents, is Mucor circinelloides [29]. It is a filamentous saprophytic fungus with action against trematode eggs (F. hepatica, Calicophoron daubneyi) [30][31], ascarids (Toxocara canis, Toxascaris leonina, A. suum, Bayliscascaris procyonis) [32][33], and whipworms (Trichuris spp.) [34]. In several investigations it was shown that M. cicinelloides can be cultivated together with D. flagrans, with ovicidal and larvicidal activity very practical for the control of helminths whose infective stages are eggs or larvae that develop in the environment [35].

2. Advances and Perspectives for the Control of Geohelminths

The nematodes A. caninum, T. Canis, and T. cati are potentially zoonotic parasites of dogs and cats in various parts of the world [36][37][38]. As part of the environmental cycle, these parasites manage to cause infections via soil/environment, giving them the name of geohelminths [39].
The use of anthelmintic drugs is the main form of control used to helminth infections in domestic animals, but cases of therapeutic failure have also been observed, resulting in reports of anthelmintic resistance [40][41][42]. It is noteworthy that the high environmental resistance of infective A. caninum larvae, T. Canis, and T. cati eggs gives them a greater ability to survive. However, by the use of helminthophagous fungi P. chlamydosporia, the environment can be used as an alternative route for their control [43][44].
In places where there is a high population of stray dogs and cats, the presence of zoonotic parasitic forms in the soil of public squares is a sanitary and environmental problem [45][46]. Children are the main affected, as they have the habit of playing on the ground [47]. The soils of public environments can be considered maintenance areas for parasites with zoonotic potential, with difficult environmental control, since restricting the access of animals to these environments is impractical. Common disinfectants such as 2% sodium hypochlorite (bleach), have highly effective in environmental sanitation, with the destruction of geohelminths in impermeable soils and surfaces. Nonetheless, common disinfectants have limitations of effectiveness on other surfaces, such as sandy soils and lawns [48][49]. Research with the purpose of promoting integrative control measures, through the association of chemical and biological control, has been developed and demonstrated satisfactory results [12][6][35][43][50][51]. Research should be encouraged to evaluate the associated use of helminthophagous fungi and common disinfectants, enabling their associated use in doses that do not cause fungal inhibition, increasing the use of these fungi.

3. Biotechnological Advances in the Use of Helminthophagous Fungi

The understanding of biotechnological advances with the use of helminthophagous fungi can be divided into two main points: predatory action against infective larvae and helminth eggs; and the production of primary and secondary metabolites [52]. In this sense, the predatory activity of helminthophagous fungi and its mechanism of action through traps and/or adhesive nets has long been recognized [15][53][54][55][56]. For this reason, the use of fungal mixtures with complementary activity (ovicide and larvicide) is of great importance. Furthermore, this mixture of fungi resists the process of manufacturing nutritional pellets and, therefore, represents a very useful formulation for the control of different helminths that affect domestic animals in grazing and wild animals in captivity [35][57].
The production of extracellular enzymes is important for understanding the mechanical and enzymatic process carried out by helminthophagous fungi, especially those classified as ovicides [52]. Through biochemical and molecular studies, it was found that there was a great possibility that these fungi produce extracellular enzymes with direct use against nematode larvae and eggs [58].
The enzymatic activity of nematophagous fungi has motivated great interest in studies in different countries. For example, in China, a recombinant protein from the species Arthrobotrys oligospora, one of the most widely studied nematode-trapping fungi, has been demonstrated to have a high chitinase activity and is able to degrade chitine from both infective stages and the egg-shell of the following helminth species Strongylus equinus, Caenorhabditis elegans, and Haemonchus contortus and also the egg-shell of the trematodes F. hepatica and Dicrocoelium chinensis [59].
Thus, research has advanced, and, recently, a new possibility of using these fungi in the control of nematodes was discovered through nanoparticles (NP’s) biosynthesized from fungal filtrate [60]. It has been proven that nanoparticles biosynthesized by D. flagrans, were able to cause the destruction of infective larvae of A. caninum [61].
The biosynthesis of these nanoparticles by filamentous fungi has attracted considerable interest for the use of these microorganisms in the production of NP’s, due to their ability to grow on low-cost, nutrient-poor substrates and to produce secondary metabolites. In addition, fungal mycelium can withstand flow pressure, agitation, and other laboratory conditions important for large-scale production. Still, in biological synthesis using fungi, the biosynthesis of NP’s occurs extracellularly. That is, the reduction occurs outside the cell, eliminating the need for extra steps to coat the NP’s in post-production [62].
Helminthophagous fungi can also produce ecological silver nanoparticles (AgNP’s) [61][60][63]. They convert toxic metal ions into non-toxic nanoparticles through their catalytic effect [64]. The destruction of L3 of equine cyatostomine nematodes by AgNP’s—D. flagrans, with nematicidal effect in 24 h, was a great advance for a new use of these fungus [6].

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Jackson Victor de Araújo
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