Introduction to Fungi, Third Edition

NEMATOPHAGOUS FUNGI
683
(group 1), credited with the highest competitiveness
in soil, forms its traps only upon induction
by the presence of nematodes, whereas producers
of knobs and rings (Dactylellina, Gamsylella
and Drechslerella; group 2) form traps more
readily but have a more limited capacity to
survive saprotrophically in soil. The obligate
end of the spectrum from saprotrophy to
parasitism among nematophagous fungi is
occupied by some of the endoparasitic fungi
(group 3). The conidia of these species form sticky
drops constitutively and have no saprotrophic
ability.
Mycelium with traps whether formed
constitutively or induced by the presence of
nematodes has been shown to attract nematodes
significantly more strongly than mycelium
without traps (Field & Webster, 1977; Jansson &
Nordbring-Hertz, 1980). The strength of attraction
can be correlated with the saprotrophic
capacity of the fungus in question, i.e. group 3
fungi exert the highest attraction to nematodes,
with group 2 fungi being intermediate and
group 1 fungi attracting nematodes to a lesser
extent even if trap formation has been induced
(Jansson & Nordbring-Hertz, 1979). The identity
of the nematode-attracting substances is as
yet unknown.
Adhesion
The strength of adhesion of a trap or conidium
to the nematode prey is remarkable, and much
work has been carried out to characterize the
glue involved. This has been summarized by
Nordbring-Hertz (1988) and Tunlid et al. (1992),
who presented evidence of the involvement of
lectins, i.e. proteins that bind to specific carbohydrate
residues (receptors). Different predatory
and endoparasitic nematophagous fungi differ
in the kind of lectin they produce, and this
may partially account for the specificity of binding
observed in some cases, e.g. in Drechmeria
coniospora whose conidia attach mainly to the
buccal end of its prey. It seems that the lectins are
located within the glue on the trap or conidium,
and that the carbohydrate-based receptors recognized
by the lectins are part of the glycosylation
chains of proteins on the nematode surface.
Toxins
The capture of a nematode by a predatory fungus
is soon followed by its death, sometimes after
a quick but violent struggle. In the case of
constricting ring traps, the stricture of the body
may well be a contributory cause of death,
but there is evidence that toxins are also
produced by certain fungi. Stadler et al. (1993)
isolated the common fatty acid linoleic acid as
a nematicidal principle of Arthrobotrys oligospora
and other species. Linoleic acid was produced
at higher amounts by trap-forming cultures
than by uninduced ones, and it was highly toxic
against nematodes in vitro, even reproducing
the typical symptoms of hyperactivity followed
by paralysis. In the case of Pleurotus spp., two
toxins have been isolated, namely trans-2-decenedioic
acid (Kwok et al., 1992) and linoleic acid
(see Anke et al., 1995). The production of antibacterial
antibiotics by numerous nematophagous
fungi has been interpreted as a substrate
defence strategy against bacterial competitors
during the colonization of a killed nematode
(Anke et al., 1995).
The infection process
Infection of nematodes often begins before
the animal is dead. Enzymatic and turgor
pressure-driven mechanisms have been implicated
(Veenhuis et al., 1985; Dijksterhuis et al.,
1990). Since the nematode cuticle consists
mainly of collagen-type proteins and because
serine proteases of the subtilisin type are known
from a wide diversity of nematophagous fungi,
these are generally assumed to play an important
role in infection of the host and its
subsequent degradation (Åhman et al., 2002;
Morton et al., 2004), and their transcription is
enhanced by the presence of nematode cuticle
(Åhman et al., 1996). A subtilisin from A. oligospora
has even been found to possess nematotoxic
properties, hinting at several roles which these
proteases may play during infection (Åhman
et al., 2002).
Details of the infection process differ between
predatory and endoparasitic nematodes. In
predatory species, penetration of the cuticle is
by means of an appressorium or a hypha emitted
by that part of the trap which is in contact