Download Underground Mycology: The Relation Between Fungi, Soil and Tree

Underground Mycology:
The Relation Between Fungi, Soil and Tree
Lynne Boddy, PhD
Cardiff School of Biosciences, Biomedical Building, Museum Avenue, Cardiff CF10
3AX
Summary
Fungi interact directly with trees as biotrophs (obtaining nutrients from living
cells/tissues) - either parasites or mutualistic mycorrhizas, and as necrotrophs (obtaining
nutrition from cells/tissues that they kill). Mycorrhizas are crucial to the health of the
vast majority of plants in nature, supplying them with water and mineral nutrients, and
protecting against root pathogens. Fungi affect trees indirectly as saprotrophs, by
decomposing dead organic matter and releasing the nutrients that were locked up
therein. The relations between fungi, soil and tree are complex since fungi also interact
with each other, with other microorganisms and with soil invertebrates affecting
mycelial growth and functioning. With changing climate the outcome of these
interactions is likely to differ, and hence the interaction between fungi and trees will
also differ.
Ecological roles of fungi
Fungi have 3 main ways by which they obtain nutrition: (1) saprotrophy, in which dead
plant, animal and microbial cells are utilised; (2) biotrophy, where nutrients are obtained
from living cells; and (3) necrotrophy, where cells and tissues are killed. Biotrophs
damage hosts when they are parasites, but others provide benefits and are mutualists.
These latter include: (1) lichens, organisms comprising a fungal partner and an algal or
cyanobacterial partner; and (2) mycorrhizas, an association between plant roots and a
fungus. These nutritional modes are not mutually exclusive: for example, many
mycorrhizal fungi have some saprotrophic ability, some mycorrhizal fungi can become
pathogenic, and necrotrophs continue to live, for variable times, following death of the
host.
Saprotrophs
Saprotrophic fungi are the major agents of decomposition (Boddy et al. 2008). In
temperate forests 12-13 tonnes per hectare of biomass is added per year as a result of
photosynthesis. In balanced systems a similar amount is decomposed to carbon dioxide
and water, with release of mineral nutrients that had been ‘locked up’ in plant tissues.
Fungi as a whole can decompose all naturally produced organic compounds, though
their individual abilities vary. Cellulose and lignin are the main components of wood
cell walls and the most abundant organic compounds on the planet. Cellulose can be
decomposed by a wide range of microorganisms, but lignins are very complex
molecules that can only be decomposed by a narrow range of microorganisms, mainly
some basidiomycetes and a few xylariaceous ascomycetes (Baldrian 2008). These fungi
are, therefore, hugely important in nutrient release and cycling in woodlands, allowing
continued productivity of plants. Moreover, they play important roles in humus
formation, soil structure and stability, provide food sources for invertebrates, and some
are biocontrol agents.
The organic resources upon which saprotrophic fungi feed are usually discrete, and vary
in size from small plant fragments and invertebrates, through leaves, twigs, branches
and stumps, to whole trees (Rayner & Boddy 1988; Fricker et al. 2008). They are
located attached to living plants, dead plants, lying on the surface of soil and within soil.
They are patchily distributed in time and space, though the leaf litter, for example, can
form a more or less continuous layer on the forest floor. For continuing survival
saprotrophic fungi must be able to spread between these resources, and this can be
achieved by spores or mycelium. Spores allow rapid spread, sometimes over long
distances, but contain relatively small amounts of nutrients. Mycelia, on the other hand,
can draw upon a larger supply of nutrients than spores when colonizing new territory.
Within organic matter, fungi spread as mycelium. Some fungi, especially cord-forming
wood decay fungi and mycorrhizal species (see below) are able to grow into soil in
search of new supplies of nutrients (Fricker et al. 2008). Some can cover several m2 or
even hectares of forest floor, and are potentially immortal. These include fungi that
colonize large patches of leaf litter on the forest floor (e.g. Collybia spp. and Marasmius
spp.), fairy-ring-formers (e.g. Clitocybe nebularis) that grow as an ever increasing
annulus of mycelium about 30 cm wide, small (e.g. Marasmius androsaceus) and large
rhizomorph formers (e.g. Armillaria spp.), and cord-forming fungi (e.g. Hypholoma
fasciculare, Phallus impudicus and Phanerochaete velutina). The cord- and
rhizomorph-formers typically extend between spatially discrete woody resources
separated by many centimeters (cms) or even meters, and can draw on resources held
within the mycelium to sustain growth; cord-formers can also absorb soluble nutrients
from soil, but insulated rhizomorphs are less able to do so. Plant matter, especially
wood, is low in nitrogen and phosphorous compared to carbon. Thus a lot of wood has
to be decomposed to provide sufficient minerals for production of enzymes and new
mycelium. Not surprisingly, therefore, saprotrophic cord-forming fungi are extremely
conservative of nutrients. Further, they adopt foraging strategies, with reallocation of
biomass, for efficient discovery of new resources (Boddy & Jones 2007). Obviously,
nutrients must be lost to soil at some point otherwise plant productivity would not
continue, but exactly when this occurs is not known. Presumably nutrients are released
when invertebrates graze on them and during mycelial battles with each other (see
below).
Biotrophic mutualists
Lichens are not quantitatively important in photosynthesis in most ecosystems. They
are, however, of major significance in some extreme environments where they may be
the major vegetation type and/or may have a crucial role in soil formation, e.g. lichen
heath. Elsewhere, lichens on rock and bare ground begin the soil formation by eroding
the rock surface and by input of organic matter from dead tissues.
Mycorrhizas, literally fungus roots, are formed by 85% of plant species including not
only angiosperms and gymnosperms, but also pteridophytes, and it therefore comes as
no surprise that there is a range of different types of mycorrhizas based on form and
function (Smith & Read 2008). Those most commonly found in trees are termed
ectomycorrhizas (ECM). Essentially they comprise a sheath of fungal material
surrounding the fine roots, to a greater or lesser extent. Some hyphae grow within the
roots, surrounding but not penetrating the root cortex cells to form a network – the
Hartig net. This is the site of exchange of sugars from the plant and water and mineral
nutrients from the fungus. This ‘swap’ forms the basis of mutualism in most
mycorrhizal relationships. The mycelium of the fungus spreads extensively in soil
enabling it to obtain water and nutrients that would be unavailable to the tree. Root
hairs are suppressed in ectomycorrhizal roots, and often the fine roots make no contact
with soil, thus the plants are entirely reliant on the fungus for water and nutrients.
Moreover, the fungal sheath and dense mycelial network in soil provide protection
against soil-borne root pathogens (see below). Also, some associations allow plants to
tolerate and colonize toxic soils, e.g. contaminated with heavy metals. The specificity of
the fungus and host varies between species. Some fungi form mycorrhizas with plants
from widely different taxa, e.g. Paxillus involutus with Pinus and Betula, whereas
others are specific to single or closely related plant species, e.g. Suillus grevilli with
Larix, and Leccinum carpinum with hornbeam (Carpinus betula). Most plants form
mycorrhizas with a range of fungal partners but some are, apparently, only mutualist
with a few species, e.g. Alnus rubra in the USA with only Alpova dipophloens and
Lactarius obscuratus.
Arbuscular Mycorrhizas (AM) are the most common and widespread type forming
with herbaceous plants, some trees, e.g. Acer, pteridophytes, and occasionally
bryophytes. Only a few plant families lack them, e.g. Cruciferae and Chenopodiaceae
(Smith & Read 2008). They are an ancient association being found in fossils from 400500 million years ago, and it is by virtue of these associations that plants were able to
colonize land. Like ECM, AM fungi form a large mycelial biomass in soil that extends
from plant roots. Unlike ECM, however, AM fungi do not form a sheath around the
roots, nor change root morphology, and they actually penetrate root cortex cells, in
which they branch profusely (forming arbuscles – ‘dwarf trees’) providing a large
surface area for the exchange of carbon, mineral nutrients and water. They have also
been implicated in protection against root pathogens.
Ericoid mycorrhizas are the third most important ecological group (Smith & Read
2008). These are associations between fungi and the fine hair roots of heathland plants
on peaty soils, e.g. heathers, Rhododendron and Vaccinium. About 80% of the volume
of root cells is packed with coils of hyphae, and these extend into the soil. Again the
fungus provides the plant with water and mineral nutrients, and the plant ‘pays’ with
sugars.
Plants in the genus Arbutus (e.g. Pacific mandrone, Arctostaphylos and several species
of Pyrolaceae form arbutoid mycorrhizas with basidiomycetes that form ECM with
forest trees. Thus, these plants are probably linked to trees via fungal mycelium, with
the potential for exchange of carbon between the two. Indeed, ECM mycelium can link
trees of different species, and sugars derived from photosynthesis in one tree have been
detected in other trees (Leake et al. 2004; Smith & Read 2008). Plants in the
Monotropaceae (e.g. Indian pipe) do not contain chlorophyll, and hence are unable to
photosynthesise. Moreover they form balls of roots that are not spread out in soils. They
form monotropoid mycorrhizas with genera such as Russula, Rhizopgon and Suillus,
which form ECM in the coniferous forests in which they grow. These monotropid plants
are thus effectively parasitic on the fungi for mineral nutrients and water, and on
coniferous trees for carbon, via the mycorrhizal mycelium! Orchids are also effectively
parasites for at least part of their lives. All orchids produce very small seeds and upon
germination must rapidly establish mycorrhizal relationships, young plants being
dependent on the fungus for not only mineral nutrients but also fixed carbon. The
achlorophyllous species are dependent on the fungus throughout their lives, i.e. they are
parasites, whereas mature chlorophyllous orchids provide fixed carbon to the fungus.
The fungi involved are wood decay basidiomycetes, e.g. species in the genera Coriolus,
Fomes and Marasmius, and pathogens, e.g. species in the genera Armillaria and
Rhizoctonia. There is a delicate balance in the relationship involving fungi that have
pathogenic ability. If insufficient sugars are provided by the orchid the balance can shift
with the fungus becoming pathogenic.
Mycorrhizas and nutrient cycling
Mycorrhizas obviously play a major role in nutrient cycling since they provide plants
with their mineral nutrients. In the past mycorrhizas were thought only to access
inorganic nutrient pools, but it is now clear that they have the ability to access organic
nitrogen and phosphorus, i.e. they have decomposer ability (Leake et al. 2004; Smith &
Read 2008). ECM are particularly good at utilizing organic nitrogen (N), which is
important in N-limited forests, e.g. many boreal forests. Its utilization short-circuits the
conventional N cycle and, by by-passing the normal mineralization pathway, it restricts
the supply of mineral N to non-ECM plants and other micro-organisms, and ACM
plants may suppress other guilds such as AM herbs and some angiosperm seedlings
whose AM fungal partners are less effective at N capture (Leake et al. 2004). Utilization
of organic N and effective scavenging of ammonium by ECM reduces flow of N
through the ammonification pathway, and thus minimises the residence time of mineral
N in soil solution and eliminates loss of N from the ecosystem through ammonium
leaching, nitrate leaching and denitrification. Addition of nitrogen in fertilizers and by
deposition from the atmosphere has resulted in the loss of some mycorrhizal fungi,
presumably because trees do not need to expend sugars on a mycorrhizal relationship
that is unnecessary when nutrients are in luxary supply. The stipitate hydnoids, for
example, are now endangered in Britain.
Parasites and pathogens
Biotrophic parasites, i.e. those fungi that obtain nutrition from living cells, tend to
parasitize aerial plant parts, e.g. the rusts and smuts. Those fungi that attack plant roots
are usually necrotrophs. Necrotrophs often attack plants that are not in possession of a
strong host defence system, e.g. immature, over mature, suppressed or otherwise
weakened, for example fungi that cause ‘damping off’. Phytophthora spp. (technically
not Fungi, but Oomycota), that are becoming increasingly troublesome (Brasier 1999),
however, colonize healthy tissues.
Root pathogens move from one host to another via spores, mycelium, aggregated
mycelial structures, such as cords and rhizomorphs, and via root contacts. For example,
Phytophthoras spread by spores, Armillaria mellea via rhizomorphs, and
Heterobasidion annosum via root grafts (Rayner & Boddy 1988).
From a tree growers perspective pathogens are a nuisance, but from the point of view of
how natural ecosystems function, pathogens are simply adding material to the
decomposition system rather sooner than usual. Plants are obviously killed in nature by
pathogenic fungi, but the problem is exacerbated when man plants extensive
monocultures. Moreover, man has caused many of our new problems. For example,
long-distance spread of Phytophthoras is often via soil or infected plant material, and
many of the more serious diseases have probably resulted from man inadvertently
introducing them to new and susceptible hosts (Brasier 1999).
Interspecific interactions
Fungi do not exist in isolation but rather continually encounter other organisms that
impact upon their growth and activity. These organisms include other fungi (Woodward
& Boddy 2008), invertebrates (Boddy & Jones 2008) and bacteria (de Boer 2008),
though the latter have been little studied. When basidiomycete mycelia meet in organic
resources their aggressive interactions may result in one fungus killing the other or a
deadlock situation in which neither makes any headway into the territory of the other,
often with the formation of interaction zone lines comprising plates formed from highly
melanised contorted hyphae. Interactions also occur when mycelia meet in soil, and can
be easily seen in laboratory soil microcosms though less easily in nature. Not only do
mycelia of the same ecological group meet, e.g. saprotroph-saprotroph interactions, but
so also do mycelia of different ecological groups, e.g. saprotroph-pathogen, saprotrophmycorrhiza and mycorrhiza-pathogen interactions.
Since many saprotrophs are more combative than pathogens, saprotrophic mycelia can
constrain the growth of pathogens. This will occur both in nature and following
manipulation by man, and is the basis of biological control (Woodward & Boddy 2008).
The classic example is application of spores of Phlebiopsis gigantea to cut stumps to
prevent colonization and spread of the pathogen H. annosum. Saprotrophic cordforming basidiomycetes also have potential to control rhizomorphic spread of
Armillaria spp.. Mycorrhizal fungi have long been known to offer protection to roots
from soil-borne pathogens. Not only does this result from the physical and antimicrobial
barrier of the ECM mycelium sheathing the root (Smith & Read 2008), but also from
the extensive extra-radical mycelium (J.R. Leake, D.P. Donnelly & L. Boddy unpub.).
Since saprotrophic and mycorrhizal mycelium are found in the upper layers of soil, they
interact (Woodward & Boddy 2008). They compete directly for easily available
nutrients and by aggressive mycelial interactions. Not only do these interactions result
in changes to the space occupied by the mycelia, but also saprotrophs can alter
mycorrhizal functioning: when mycelium of the saprotrophic cord-forming
basidiomycete interacted with that of Paxillus involutus and Suillus bovinus allocation
of photosynthate from the plant to the mycorrhizal mycelial tips was inhibited by
Phanerochaete velutina (Leake et al. 2001). Nutrients may even be released to soil.
Certainly, when saprotrophic mycelia meet each other nutrients are released into the
soil, not only in the interaction region, but also elsewhere in the mycelium (J.M. Wells
& L. Boddy unpub.). Further, decomposition rate of wood sometimes increases during
interactions, and sometimes decreases (Woodward & Boddy 2008). These interactions
could clearly alter nutrient uptake by trees, and nutrient recycling.
Soil invertebrates often graze on fungal mycelia either directly or incidentally while
ingesting colonized organic material. Fungal mycelia contain massively greater
concentrations of nitrogen and phosphorus than does wood and even leaf litter, and is
thus highly nutritious. Grazing by collembola dramatically alters mycelial morphology
and growth rate, sometimes causing increases and sometimes decreases (Boddy & Jones
2008). Rate of wood decomposition and hence of nutrient cycling can also be affected,
and nutrients are probably released during invertebrate grazing. Moreover, the outcomes
of interspecific mycelial interactions can also change as a result of grazing (TD
Rotheray, TH Jones & L. Boddy unpub.). This could have further repercussions for the
composition of fungal communities, decomposition processes and nutrient cycling.
Mycorrhizal fungi are also food for invertebrates, and grazing can disrupt the flow of
carbon through mycorrhizal mycelia (Johnson et al. 2005).
Conclusions
Fungi are crucial to tree health. The relationship between fungi and trees is, however,
likely to alter as climate changes. Temperature and moisture regime are major
determinants of decomposition rate and hence of nutrient cycling. The optimum
temperature for growth and metabolism of most fungi in temperate ecosystems lies
between 25-35ºC. Clearly, most decomposer fungi experience suboptimal temperatures
most of the time. Thus, increase in temperature, as a result of climate change, may
result in an increased rate of fungal growth and organic matter decomposition, but only
if sufficient water is available. Abiotic environment, however, affects the outcome of
interactions between fungal mycelia, thus climate change is likely to affect the
composition of fungal communities in soil and dead organic matter. Likewise
mycorrhizal relationships may also alter. Currently, we have insufficient knowledge to
understand what changes will occur and how these will affect decomposition processes,
other aspects of ecosystem function and tree health.
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