Introduction to Fungi, Third Edition

452 LICHENIZED FUNGI (CHIEFLY HYMENOASCOMYCETES: LECANORALES)
carbohydrate is added. This will saturate the
uptake system of the mycobiont; only if it is
identical to the radiolabelled mobile carbohydrate
exported by the photobiont will the latter
accumulate in the incubation medium, where
its radioactivity can be measured. Such studies
have shown that cyanobacterial photobionts
export glucose to the mycobiont, whereas green
algae export polyols such as erythritol (Trentepohlia),
sorbitol (Hyalococcus, Stichococcus) or ribitol
(Trebouxia, Coccomyxa, Myrmecia) (Ahmadjian,
1993). Tapper (1981) estimated that at least 70%
of the total photosynthetically fixed carbon is
transferred from the photobiont to the mycobiont
in Cladonia convoluta. Once taken up by the
fungus, the transport carbohydrate is rapidly
converted to mannitol (Lines et al., 1989;
Ahmadjian, 1993).
Cultured algal photobionts do not secrete
polyols into the medium, and if they are separated
from a fresh lichen thallus, polyol secretion
ceases within a few hours. Nothing appears
to be known about the mechanism by which
carbohydrate export from the photobiont is
regulated (Ahmadjian, 1993). Contact of the
mycobiont with its photobiont partner takes
various shapes. The gelatinous extracellular
sheath of cyanobacteria is penetrated by hyphal
protrusions, whereas direct wall-to-wall contact
occurs between mycobionts and green algal
photobionts. Appressorium-like structures presumably
facilitate attachment, and haustoria
may also be formed within the photobiont cells
especially in simple, non-stratified crustose
lichens (Fig. 16.3c). In more highly differentiated
lichens, haustoria are often reduced to a pad-like
infection peg appressed to but not breaking the
algal wall (Fig. 16.3d). Such structures have been
called intraparietal haustoria (Honegger, 1986).
Fungal hyphae and attached photobiont cells
are often coated by hydrophobin-type proteins
and other hydrophobic molecules secreted by the
mycobiont (Honegger, 1997; Scherrer et al., 2000).
Thus, the main transport route from the photobiont
to the mycobiont, in the absence of large
haustorial interfaces, must be through the
apoplast by cell wall contact (Ahmadjian, 1993).
This is different from the elaborate membraneto-membrane
contact as found in the haustorial
complexes of arbuscular mycorrhizal fungi (see
Fig. 7.46c) and biotrophic parasites (see Fig. 13.5).
The reason for the reduction in membrane
contact in the lichen symbiosis may lie in the
fact that membranes are among the most easily
damaged structures during the drying and rehydration
cycles to which lichens are exposed.
Large haustoria might thus reduce cell viability.
Presumably sufficient carbohydrate leaks out
of the photobiont cells during the frequent
drying rehydration cycles without the need for
intracellular haustoria (Honegger, 1997).
Fungi with a cyanobacterium as their primary
or secondary photobiont benefit by receiving
nitrogen in addition to carbohydrates. Nitrogen
fixed by cyanobacterial photobionts is released
to the mycobiont as ammonium (NH þ 4 ) and
is incorporated into the amino acid pool as
glutamate (Nash, 1996b).
Whilst the advantages of the lichen symbiosis
to the mycobiont are obviously nutritional, there
is no clear evidence of the transfer of any
minerals or other nutrients from the mycobiont
to the photobiont. The benefits to the photobiont
may include the buffering against adverse
environmental conditions such as high solar
irradiation. The upper cortex of many lichens is
brightly coloured due to the presence of
pigments which screen out UV light (see Plate
8b,c). In fact, cortical pigments may filter out as
much as 50% of the incoming light, and this is
particularly important with Trebouxia spp. as
photobiont because these algae favour low light
intensities (Masuch, 1993). Lichen thalli growing
at higher altitudes or on surfaces facing
the sun often contain higher pigment concentrations
than less-exposed thalli. An example of a
light-screen pigment is the polyketide usnic acid
(Fig. 16.5) which is also toxic against bacteria,
fungi and other organisms (Elix, 1996; Cocchietto
et al., 2002). This substance is produced by several
taxonomically unrelated lichens, but has not yet
been isolated from any non-lichenized fungus.
Another example is the pulvinic acid derivative
vulpinic acid (Fig. 16.5) produced by the wolf’s
lichen, Letharia vulpina. This species is so toxic
that its thalli have been used in the past to
poison foxes and wolves, by laying out animal
carcasses spiked with ground lichen thalli