Nematophagous Fungi

Abstract

Nematophagous fungi are microfungi that can capture, kill and digest nematodes. They use special mycelial structures, the so‐called traps, or spores to trap vermiform nematodes or hyphal tips to attack nematode eggs and cysts before penetration of the nematode cuticle, invasion and digestion. The more than 200 species known differ in saprophytic/parasitic ability. Although many of the trap‐forming and egg‐parasitic fungi can survive in soil saprophytically, the endoparasites are mostly more dependent on nematodes as nutrients. Molecular data have greatly improved our understanding of the function of the fungi in respect of their taxonomy, their physiological/biochemical activity and their ecology, including their function as biocontrol agents.

Key Concepts:

  • There are three major groups of nematophagous fungi: the nematode‐trapping fungi that capture free‐living nematodes using specialised morphological structures (i.e. traps), the endoparasitic fungi that infect nematodes using adhesive spores, and the egg‐ and cyst‐parasitic fungi that infect these stages with their hyphal tips.

  • The nematophagous growth habit has evolved several times and independently since nematophagous fungi are found in all major groups of fungi.

  • The nematophagous fungi display a large diversity and extensive plasticity of infection structures. In many species, the formation of trapping‐structures is initiated in response to signals from the environment including compounds secreted by the host nematode.

  • Isolation of more virulent strains, and the development of better formulations and fermentation techniques have significantly improved the efficiency of nematophagous fungi as biological control agents against plant‐ and animal parasitic nematodes.

  • Nematophagous fungi infect nematodes through a sequence of events including adhesion of the trapping structures to the host nematode surface, followed by penetration, killing and digestion of the nematode tissues.

  • The secretion of extracellular enzymes such as serine proteases and chitinases are required for successful parasitism of free‐living nematodes and nematode‐eggs by nematophagous fungi.

Keywords: nematode‐trapping fungi; endoparasitic fungi; adhesion; penetration; digestion; Evolution of fungal parasitism; egg‐parasitic fungi

Figure 1.

Diversity of trapping structures in nematophagous fungi. (a) Nematode trapped (arrow) by Arthrobotrys oligospora. Bar, 100 μm. Reproduced from Nordbring‐Hertz B, Zunke U, Wyss U and Veenhuis M (1986) Trap Formation and Capture of Nematodes by Arthrobotrys oligospora. Film No C1622. Courtesy of IWF Wissen Und Medien GmbH i.L, Göttingen. (b) Adhesive network of A. oligospora, developed from digested nematode. Bar, 20 μm. (c) Adhesive branches of Monacrosporium gephyropagum. Bar, 10 μm. (d) Adhesive knobs of Monacrosporium haptotylum. Bar, 10 μm. (e) Constricting ring of Arthrobotrys brochopaga. Bar, 5 μm. (b–e) Reproduced from Nordbring‐Hertz et al.. Courtesy of IWF Wissen Und Medien GmbH i.L, Göttingen. (f) Nematode infected by conidiospores of Drechmeria coniospora. Bar, 5 μm. Reproduced from Jansson H‐B (1982) Attraction of nematodes to endoparasitic fungi. Transactions of the British Mycological Society79: 25–29. Courtesy of the British Mycological Society. (g) Dr. coniospora spores with adhesive buds (arrows). Bar, 10 μm. (h) Zoospores of Catenaria anguillulae. Bar, 10 μm. (g–h) Reproduced from Nordbring‐Hertz et al.. Courtesy of IWF Wissen Und Medien GmbH i.L, Göttingen.

Figure 2.

Trapping of nematodes by Arthrobotrys oligospora. (a) Scanning electron micrograph (SEM) of peptide‐induced adhesive network. Bar, 10 μm. Reproduced from Lysek G and Nordbring‐Hertz B (1983) Die Biologie der nematodenfangender Pilze. Forum Mikrobiologie6: 201–208. Courtesy of G‐I‐T Verlag Ernst Giebeler, Darmstadt. (b) Transmission electron micrograph (TEM) of vegetative hypha (upper panel) and a trap cell. Bar, 1 μm. Note dense bodies only in the trap cell. Reproduced from Nordbring‐Hertz B (1984) Mycelial development and lectin–carbohydrate interactions in nematode‐trapping fungi. In: Jennings DH and Rayner ADM (eds) The Ecology and Physiology of the Fungal Mycelium, pp. 419–432. Courtesy of Cambridge University Press. (c) TEM of adhesive A. oligospora. After capture of the nematode the fibrils (F) of the adhesive becomes directed from the trap (T) towards the nematode cuticle (NC). Bar, 1 μm. (d) TEM of penetration of nematode cuticle by A. oligospora. Note electron dense bodies (DB), adhesive coating (A), nematode cuticle (NC) and infection bulb (IB). Bar, 1 μm. (c and d) Reproduced from Veenhuis M, Nordbring‐Hertz B and Harder W (1985) An electron microscopical analysis of capture and initial stages of penetration of nematodes by A. oligospora. Antonie van Leeuwenhoek51: 385–398. Courtesy of Kluwer Academic Publishers, Dordrecht.

Figure 3.

A phylogenetic tree based on the sequences of 18S rDNA showing the relationships among the nematode‐trapping fungi and the position of this clade among species from the Pezizales (P), Leotiales (L) and Calciales (C). Neolecta vitellina was used as an outgroup for the analyses. Note that the phylogenetic pattern is concordant with the structure of the trapping devices. Orbilia auricolor is the teleomorph (sexual stage) of Arthrobotrys oligospora. Reproduced from Ahrén et al.. Courtesy of Federation of European Microbiological Societies.

Figure 4.

Trapping mechanism of constricting rings of Arthrobotrys brochopaga. (a–c) Closure of a ring triggered by applying heat to the trap. The closure is rapid (0.1 s), irreversible and is accompanied by a large increase in cell volume leading to an almost complete closure of the aperture of the trap. Bars, 5 μm. (d) Nematode firmly captured in a ring. Bar, 10 μm. Reproduced from Nordbring‐Hertz et al.. Courtesy of IWF Wissen Und Medien GmbH i.L, Göttingen.

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Further Reading

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Nordbring‐Hertz, Birgit, Jansson, Hans‐Börje, and Tunlid, Anders(Nov 2011) Nematophagous Fungi. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000374.pub3]