FUNGAL ECOLOGY
(sometimes with special regard to macromycetes)
Fungi and their environment • Life strategies and interactions of fungi • Ecological groups of
fungi, saprotrophs (terrestrial fungi, litter and plant debris, wood substrate, etc.) • Fungal
symbioses (ectomycorrhiza, endomycorrhiza, endophytism, lichenism, bacteria, animal relationships)
• Parasitism (parasites of animals and fungi, phytopathogenic fungi, types of parasitic relations)
• Fungi in various habitats (coniferous forests, broadleaf forests, birch stands and non-forest
habitats, fungal communities)
• Fungal dispersal and distribution • Threat and protection of fungi
(the study material has not been corrected by native speaker)
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MASARYK UNIVERSITY, FACULTY OF SCIENCE
DEPARTMENT OF BOTANY AND ZOOLOGY

LICHENISM
Lichenism is a strong, stable and self-sufficient relationship between fungi (mycobiont) and algae
or cyanobacteria (this component is called a phycobiont or cyanobiont, respectively, or generally a
photobiont).
The photobiont supplies its partner with assimilates, while the mycobiont provides a source of
water and minerals for the photobiont – so it is not a one-sided „exploitative“ relationship.
In addition, for heteromeric thalli (divided into layers: upper cortical, gonidial with photobiont
cells, medullary, or even lower cortical with rhizines on the underside), the mycobiont determines
structure of the thallus and provides protection of the photobiont cells against impact of the
environment. The upper cortex is of paramount importance as a protection against desiccation, which
can be increased by pigmentation of the tissue.
The situation is different in homeomeric thalli (not divided into layers, in the whole volume the
cyanobiont cells are scattered among the mycobiont hyphae), where the structure is determined by
the cyanobiont, which also secretes polysaccharides capable of absorbing and retaining water (the
thallus resembles mucoid colonies of cyanobacteria).
Lichens with cyanobionts are also able to fix nitrogen gas (N2), while balancing the phosphorus
balance, creating growth substances and substances allowing the lichen to grow into the substrate
are more provided by the mycobiont.

Reproduction of lichens is mostly vegetative, more rarely mycobiont is forming fruitbodies and
spores. In the case of the fruitbody formation, the so-called hymenial gonidia can enter the
thecuim – photobiont cells, which adhere to the released ascospores.
Different ways of vegetative reproduction are the result of an effort to compen-sate for the low
probability of mycobiont spores encounter with the partner's cells – it is a separation of
different parts of the thallus (leprose stage) or formation of surface structures such as soredia,
isidia, schizidia or phyllidia. /More about lichen thalli in General mycology, in the chapter
Vegetative thallus of fungi./
In heteromeric thalli, photobiont reproduction is suppressed (algae or cyanobacteria must be
cultivated to detect them), while in the case of homeomeric lichens, the photobiont can grow out
from the thallus and reproduce or become independent of the fungus.
On lichen thalli we can also find fungal parasites (lichenicolous fungi) or para-symbionts (there
is no sharp border between these categories). Parasymbiotic fungi are those that live freely (i.e.
not in an obligatory relationship), but can enter the lichen symbiosis as an occasional partner
(and leave it at any time).
Symbioses are also known at the level of „fellowship“, as well as balanced (mutualistic) and
unbalanced symbioses with a tendency to parasitism – many cases of lichenism basically begin as a
parasitic relationship, while others gradually turn to parasitism. Cases of lichen „divorce“ have
also been observed, what results in (at least temporary) independent existence of its components.

In nature, the behavior of a lichenised fungus was observed on the surface of rocks, where it grows
next to colonies of their partner algae or cyanobacteria => fungal hyphae grow to photobiont cells,
around which they form mucus and cover
C:\Documents and
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them in close contact, and no antibiotic effect was observed – the theory, that lichens evolved as
a result of similar interactions, is based on this finding.
Under laboratory conditions, lichen was synthesized only in the second half of the 20th century:
mixing a pure culture of fungus (Cladonia cristatella) with algal culture (Trebouxia glomerata) =>
hyphae overgrow algal cells => nodules =>
aggregation
=> thallus
scales formed
after about
2 months => fruitbodies formation after some time => complete podetia in about a year.
C:\Documents and
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Cladonia cristatella

In nature, the lichen growth is significantly slower, lichens are considered to be the slowest
growing organisms – growth of the thallus is usually 0.5–2.5 mm in crustose, 1–6 mm in foliose and
fruticose species, at most about 15 mm per year.
Age of lichen thalli corresponds to this – they are usually hundreds of years old; crustose
lichens, especially in cold regions, can be up to thousands of years old.
Lichens belong to „S“ strategists (stress tolerant) with limited competitive ability (this fact is
related to slow growth, in addition, lichens do not tolerate shading too much), which can be found
in extreme conditions from the tropics (drought in arid regions) to the polar regions (low
temperatures).
However, mycobionts of some species also produce antibiotic substances (significantly stronger than
common antibiotics), which make them „C“ strategists in principle.
They play an important role in colonising new habitats – among their metabolites we find acids that
can disrupt the mineral substrate („corrosion“ of the substrate, such as limestone rocks) and
release mineral compounds from it for further use by lichens (to a lesser extent; solutions in
run-off rainwater or surface water are usually sufficient for them) and for needs of other plant
„colonisers“.

Most lichenised fungi belong to the division Ascomycota (especially the class Lecanoromycetes)
including imperfect fungi (for which the perfect = ascospore stage is not known); a few percent of
the species are then found independently scattered in different groups of the class Agaricomycetes
(Basidiomycota).

A specific case is Geosiphon pyriforme (Glomeromycota), which contains symbiotic cyanobacteria of
the genus Nostoc in its thallus (as demonstrated by cultivation). Some lichenologists also classify
this organism as lichenised fungus
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while opponents of this concept argue that it is not a lichen thallus of the heteromeric or
homeomeric type – localisation of the symbiont cells corresponds to the definition of endocyanelles
as known in some groups of algae (Glauco-phyta, some Dinophyta). Since all species of Glomeromycota
have an endomycorrhizal relationship, in this case it may be a combination of two types
of symbiosis.
Milan Gryndler et al.: Mykorhizní symbióza, Academia, Praha, 2004.
Photo Arthur Schüßler.

Lichens are known as indicators of air pollution; by absorbing practically all substances dissolved
in the running water, in their tissues they store compounds which cause dying of the thalli. They
are most sensitive to sulphur dioxide, changing chlorophyll to non-green pheophytin => loss of the
photosynthetic ability leads to death of the whole organism (externally it is manifested by colour
change and gradual disintegration of the thallus).
Such indicators are only some species, it is not
possible to apply this role to all lichens – the most
sensitive are epiphytic (tree) lichens with fruticose,
eventually foliose thallus (Usnea, Alectoria, Evernia,
Lobaria), ...
69_usnea_longissima 70_Alectoria_ochroleuca 71_Evernia_prunastri 72_lobaria_pulmonaria
Centre: Alectoria ochroleuca (Ulrich Kirschbaum,
http://kmubserv.tg.fh-giessen.de/pm/page.cfm?PRID=20&CFID
=86688&CFTOKEN=154363&PID=901),
right: Evernia prunastri
(Photo Fred M. Rhoades,
http://faculty.wwu.edu/fredr/Lichen_table.htm)
Photo Josef Hlásek, http://www.hlasek.com (2x)
Lobaria
pulmonaria
Usnea longissima

... on the contrary, species of the genera Lecanora or Hypogymnia can be classified as tolerant.
In nature, there may be places with specific pollution, for example with a high concentration of
some metals, where species tolerant to these metals can selectively succeed; on the contrary, in
cities the pollution is usually „complex“, so the spectrum of lichen flora is significantly
limited.
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C:\Documents and
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Left: Lecanora muralis, right: Hypogymnia physodes
Photo Ivo Antušek, http://www.biolib.cz/cz/image/id9453/
http://www.cwikowscy.pl/powiekszenie.php?kategoria=7&nr=1

In addition
to lichenism,
there are also looser interactions between different species of fungi and algae – for example,
different Trametes species, whose fruitbodies tend to be colonised by algal cells over time (not
only on the surface, sometimes entering deep into the tissues), or corticioid fungi growing on the
surface of wood previously colonised by algae; species of the genus Athelia thus pass to direct
parasitism, the penetration of haustoria and killing of algal cells – not only of free algae, but
also of lichen photobionts (observed on Lecanora conizaeoides).
C:\Documents and
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anobacteria.jpg
Clémençon: Cytology and Plectology of the Hymenomycetes, 2004.

The mentioned cases are usually „accidental and irregular encounters“, but there are also frequent
coexistences such as Resinicium bicolor with chlorophyte Coccomyxa glaronensis – although it is not
obligatory lichenism, fungal structures or algal cells are not morphologically adapted, the algal
cell involvement in the fruitbody tissue is referred to as „physiological lichenism“.
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Heinz Clémençon: Cytology and Plectology of the Hymenomycetes. Bibliotheca Mycologica 199.
J. Cramer, Berlin-Stuttgart, 2004.

INTERACTIONS WITH BACTERIA
Cyanobacteria in lichens are not the only prokaryotes in which a relationship with fungi has been
observed – during the 20th century, coexistence with bacteria was discovered (first in some
gasteromycetes, later also in other groups of fungi). It can be assumed that mutual interactions
(as well as competition for resources) have been here since living organisms became terrestrial.
Bacteria are abundant in the rhizosphere, on the hyphal surface, but also inside the hyphae. They
are also present in mucoid colonies inside the tissues (in the
C:\Documents and
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space between the hyphae), or in the mucus layer on the surface of the fruitbodies (ixocutis); in
larger quantities they occur, for example, in the fruitbodies of Hydnum rufescens or Cantharellus
cibarius, where they seem to „help“ in the fruitbody development.
Heinz Clémençon: Cytology and Plectology of the Hymenomycetes. Bibliotheca Mycologica 199.
J. Cramer, Berlin-Stuttgart, 2004.

Together with fungi, bacteria are involved in the degradation of root exudates (the original ideas
even attributed this role exclusively to bacteria). As 13C has shown, fungi are most involved in
the degradation of exudates in acidic soils and at high concentrations of exudates (they better
tolerate osmotic stress), otherwise competition (associated
with excretion of anti-fungal,
anti-bacterial and non-specific
substances) is to be expected.
Some bacteria manifest as mycophagous. Spore penetration and wrapping of Streptomyces chains around
the hyphae were observed; species of this genus are also the main decomposers of dead hyphae in
soil. The genus Collimonas has recently been found to attack fungal hyphae in acidic soils and to
penetrate their walls with a mixture of enzymes (chitinases, proteases). A specific case is
myxobacteria (G–), which commonly feed on other bacteria and yeasts („micropredators“), but their
motile mucoid colonies have been seen attacking the hyphae of Rhizoctonia sp.
Some bacteria are mycoparasitic (e.g. Pseudomonas tolaasii on Agaricus bisporus).
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„Dirt“ among dark hyphae of the genus Rhizoctonia (see also a more detailed picture of monilioid
cells in orchid mycorrhiza) are ubiquitous bacteria.
Gryndler et al.: Mykorhizní symbióza, Academia, Praha, 2004.

During decomposition of lignocellulosic complex,
simple sugars and phenolic compounds are
formed – the interactions that occur here can be
mutualistic, commensal or even competitive:
– bacteria utilise nutrients without fungus suffering,
while they are producing vitamins, growth factors,
fixing nitrogen, breaking down toxic metabolites;
– bacteria utilise nutrients without fungus suffering;
– bacteria utilise nutrients and „rob“ the fungus.
Growth of bacteria and actinomycetes on lignin
has also been observed in vitro, but under
natural conditions their proportion is negligible
and lignin degradation is a matter of fungi. Also
aerobic decomposition of cellulose is mainly
a matter of fungi, but in anaerobic conditions
(with the exception of Neocallimastigales, see
below) bacteria are involved (Acetivibrio, Clostridium). Aerobic bacteria and actinomycetes need
higher pH than fungi – they succeed e.g. in composts, where the pH increases by ammonification (but
there is also competition of fungi and bacteria), while in soil they occur only opportunistically
(they probably do not have sufficient antifungal substances) and in wood minimally (it is an acidic
substrate itself, into which the fungi also excrete organic acids).
Different positive/negative affect of bacteria on growth of different fungi
taken from http://botany.natur.cuni.cz/koukol
/ekologiehub/EkoHub_5.ppt
Source:
Lang et al. 1998

A specific niche for bacteria is the surface of hyphae, where they utilise mannitol and trehalose
(Pseudomonas) or organic acids (Methylobacterium, Streptomyces).
Bact_hyph
The production of fungal substances has not yet been quantified here, but apparently the fungi
affect the qualitative spectrum more than the quantity of bacteria, while the selection of bacteria
resistant to fungal antibiotics (G+ versus G–) is also evident.
Different communities can be found in the rhizosphere without mycorrhiza and in mycorrhizosphere
due to different production of fungal exudates and stimulation of the plant exudation.
Group of species mainly of the genus Pseudomonas represents the so-called „ECM helper bacteria“ –
they stimulate
the formation of mycorrhizal symbiosis and the growth of ectomycorrhizal fungi (the mechanism of
action remains unknown). Some of themalso have an effect on fructification (Agaricus bisporus,
Pleurotus ostreatus + Pseudomonas putida), in other cases the fungus benefits from the interaction
with the plant and nitrogen-fixing bacteria (community with mycorrhiza of Rhizopogon vinicolor +
Pseudotsuga).
http://soils.usda.gov/sqi/concepts/soil_biology/bacteria.html (published there with permission of
Cambridge University Press)

Source: R. Campbell:
Plant Microbiology. Edward Arnold, London, 1985

Arbuscular fungi do not have association with true „helpers“, but there is positive effect of fungi
and bacteria on the plant, the spread of bacteria on the mycelium (Rhizobium leguminosarum +
Gigaspora margarita) or the germination of spores of mycorrhizal fungi if antifungal substances are
degraded (on the other hand, their production has a negative effect on the spore germination =>
induction of mycostasis or fungistasis).
C: SEM photo of Gigaspora decipiens
hyphae (H), Burkholderia pseudomallei
(arrows) and fibrillar material. D: Semi-thin section of G. decipiens hypha inoculated by
B. vietnamiensis; stained by toluidine blue. Bacteria (arrows) are present everywhere in the
cytoplasm (CW = cell wall). E: TEM photo of bacteria in the cytoplasm of G. decipiens (arrows).
Since the 1970s, „bacteria-like organelles“ had been observed inside the hyphae of arbuscular fungi
in electron microscopic images, in which bacteria were recognised (non-cultivable, identified to
species by PCR), most often of the genus Burkholderia (the original idea,
that they help with nitrogen fixation,
has not been confirmed). Probably
a symbiotic event happened only
once, followed by vertical
transmission.

The transfer of bacterial cells appears to take place through the spores, and entry into the
mycelium can occur when the wall of the germ tube is disrupted by lytic enzymes. Otherwise, the
„absorption“ of bacteria is difficult due to strength of the cell wall and it can occur only at the
tip during hyphal growth (this mechanism also has Geosiphon pyriforme + Nostoc; there is something
like phagocytosis and formation of vesicles at the tips of the hyphae).
By the way, bacteria of the genus Burkholderia are common colonisers of the rhizosphere that can
utilise almost anything (they even degrade halogen derivatives). Their coexistence with other
organisms can take various forms (beneficial to plants or parasitic) and they can attack eukaryotic
cells and survive as intracellular parasites (observed in amoebae, but also in macrophages,
epithelial cells); pathogenic effects on animals, including humans, are also possible (e.g. B.
cepacia and B. pseudomallei can kill people with weakened immunity, after application of
antibiotics or e.g. with cystic fibrosis).
B_cepacia
http://www.apsnet.org/online/Archive/1998/cepacia.htm
B_cepacia2
Burkholderia cepacia and symptoms of its action in onions
Photo Janice Carr,
http://en.wikipedia.org/wiki
/File:Burkholderia_cepacia.jpg